An overview of Chara L. in Australia (Characeae ... - CSIRO Publishing

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Australian Systematic Botany 18, 25–39

An overview of Chara L. in Australia (Characeae, Charophyta) Michelle T. Casanova Royal Botanic Gardens, Melbourne, RMB L620 Westmere, Vic. 3351, Australia. Email: [email protected]

Abstract. Charophytes (family Characeae) are a cohesive group within the green algae. The genus Chara is abundant and diverse in a variety of Australian habitats. Approximately 37 taxa of Chara have been described on the basis of Australian collections. The current status of charophyte taxonomy is confused. RD Wood revised Australian charophytes in 1972 on the basis of an erroneous species concept, and charophytes are rarely identified lower than genus by ecologists and water managers. Many species were described by overseas experts in the mid-1800s, and this trend continues to the present day. Typically, species descriptions have been based on examination of few specimens, and sometimes not even fertile representatives of each species. In this study Wood’s (1972) taxonomic treatment of Australian members of the genus Chara is examined and analysed in relation to historical species concepts and more recent experimental taxonomy and oospore morphology. Thorough studies based on determination of reliable indicators of genetic incompatibility through culture studies, including oospore morphology and genetic analysis and objective analysis of fertile specimens, are now required.

Introduction Limnologists and aquatic botanists in Australia will be familiar with family Characeae (commonly called charophytes), a group of macroscopic green algae that grow in fresh, brackish and saline non-marine waters throughout Australia (and the rest of the world). They are similar in appearance to the submerged angiosperms Myriophyllum and Ceratophyllum, with long axes and whorls of leaflike structures (branchlets) at the nodes. However, their basic construction consists of large, multinucleate, haploid cells joined end-on-end, and each node has a complex of branchlets and accessory cells. Their sexual reproductive organs (oogonia and antheridia) are also different from angiosperm flowers. They can reproduce vegetatively (by bulbils and contracted, starch-filled branches) and sexually through diploid oospores. They can be annual or perennial, but most collectors would agree that they are unreliable in their occurrence. Reproductive organs can be ephemeral also, so collecting a charophyte with oogonia, antheridia and oospores can be a lucky occurrence. Consequently, only about 60% of specimens in Australian herbaria are sufficiently mature to be used in a taxonomic study. Five of the six recognised genera of charophytes occur in Australia, Chara L., Nitella Ag. em. A. Braun, Lamprothamnium J. Groves, Lychnothamnus (Rupr.) Leonh. and Tolypella (A. Braun) A. Braun. Australian charophytes suffer from a long and confusing taxonomic history. The first Australian charophytes to be described were collected by Robert Brown, © CSIRO

29 March 2005

Chara australis R. Br. and Nitella congesta (R. Br.) A. Braun. (Brown 1810). Early collectors like Gunn, Preiss and Drummond (Braun 1849) included charophytes in their exsiccatae and Ferdinand von Mueller encouraged collectors and was an avid collector himself. Most of the specimens collected were sent to Alexander Braun in Germany (e.g. Braun 1843, 1849, 1852). When Braun died, Otto Nordstedt became the overseas expert (Braun and Nordstedt 1882; Nordstedt 1891, 1918), followed by James Groves and GO Allen in Britain (Groves and Allen 1935) and eventually, Richard Wood. Wood came from Rhode Island on a Fullbright Scholarship to collect and examine Australian charophytes to complete his world monograph (Wood and Imahori 1965) and was the first of these specialists who actually visited Australia and saw live material. Before Wood’s visit, Beth Williams (nee Macdonald) worked on Australian charophyte taxonomy (Macdonald and Hotchkiss 1956; Chambers and Williams 1959; Williams 1959), until her work was interrupted by the Armidale fire. The most recent monographic treatment was undertaken by Joop van Raam, working in The Netherlands, who revised the charophytes of Tasmania after a collecting visit (van Raam 1995). Other local species have been described by Hotchkiss and Imahori (1988), Garc´ıa (1996) and Garc´ıa and Casanova (2004), and distributional studies have been undertaken (Brock and Lane 1983; Brock and Sheil 1983; Casanova 1993; Garc´ıa 1999; Casanova 2004a, 2004b; Casanova and Dugdale 2004). Many specimens deposited in German herbaria have been lost, presumably during the bombing of Berlin, and 10.1071/SB04027

1030-1887/05/010025

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Australian Systematic Botany

the accumulated collections from Australian herbaria were largely damaged or destroyed in the Armidale fire in 1958 (Wood and Williams 1967). Early accounts recognised the high degree of endemism and uniqueness in Australian Characeae (e.g. Braun 1849; Nordstedt 1891). Wood’s taxonomy Wood revised the Characeae of the world in 1965 (Wood 1965). He reduced many formerly described species to varieties and forms for several reasons. First, he thought that most vegetative characters were very variable. Charophytes, being submerged aquatic plants, are responsive to the physical and chemical characteristics of the water in which they grow. Wood placed great value on culture studies that showed that long-term culturing could induce morphological changes (e.g. Corillion 1957). Previous taxonomists appear to have described every morphological variation as a separate species or variety (e.g. Braun and Nordstedt 1882), but Wood thought that many of these morphologies were flexible, rather than fixed. Consequently, he united many taxa that were morphologically similar, or in which he could see a continuum of variation. Second, Wood misinterpreted the results of some breeding studies done in Australia (Macdonald and Hotchkiss 1956) believing that their results showed that crosses between dioecious and monoecious entities produced viable offspring (Wood 1965: 19, 27), when in fact only dioecious entities were used (Macdonald and Hotchkiss 1956). Third, he thought that ‘if all the microspecies were to become established, and if each genotype were to be described and named, the numbers could become truly formidable’ (Wood 1965: 763). So, on the basis of morphological flexibility and conspecificity of monoecious and dioecious taxa he reduced 116 species of Chara to 18, approximately 180 species of Nitella to 49, several species of Lamprothamnium down to three, 13 species of Tolypella to two, five species of Nitellopsis to three, and retained one species of Lychnothamnus (Wood 1965). At a local level, he reduced some 95 species in Australia to approximately 30, amalgamating many Australian species with those on other continents (Wood 1972). Within the genus Chara 37 taxa were amalgamated into 10 species (Table 1), leaving a single endemic species of Chara. Challenges to Wood’s taxonomy The characters used in taxon delineation by Wood (Table 2, characters 1–11) were based more on tradition than science (Proctor 1975, 1980). Thus the major challenge to Wood’s taxonomy focused on scientific analysis of reliable characters (McCracken et al. 1966; Proctor 1970, 1971; Grant and Proctor 1971; summarised in Proctor 1975). Citing the need for an objective set of criteria for species delimitation in cryptogams, Proctor initiated a huge number of breeding experiments in Chara which showed that sexual characters (monoecy, dioecy, the arrangement of gametangia, type

M. T. Casanova

of antheridia, number of chromosomes) and distribution (Table 2, characters 12–16) were good indicators of genetic isolation, and also that there were more discrete taxonomic entities (species) than Wood recognised. Consequently during the latter part of Wood’s career, he started to doubt some of his earlier decisions, suggesting, for example, that perhaps the name Chara australis R. Br. should be retained for dioecious entities of Chara corallina Kl. ex. Willd., em R. D. Wood in New Zealand (Wood and Mason 1977). More recently, surveys of oospore characteristics (John and Moore 1987; John et al. 1990; Leitch et al. 1990; Casanova 1991, 1997; Soulié-Märsche 1999; Sakayama et al. 2002) and genetic analysis (McCourt et al. 1999; Meiers et al. 1999; Karol et al. 2001) have produced evidence that Wood’s taxonomy was flawed. Oospore variation Oospores of charophytes are thought to have taxonomic significance (John and Moore 1987; John et al. 1990; Leitch et al. 1990; Casanova 1991, 1997; Sakayama et al. 2002) especially in the genus Nitella. Although Wood (1965, 1972) did not consider them useful, he did provide descriptions and illustrations of their variation (Imahori and Wood 1965). For the genus Chara, Proctor and Wiman (1971) found that oospore morphology differed among genetically distinct entities, and oospore colour had some taxonomic significance (Proctor 1975). John et al. (1990) provided new characters to use in assessing Chara oospores, and Casanova (1997) found that while the length to width ratios could vary somewhat within a taxon, depending on its ecology, the overall morphology and fine detail of the oospore wall could be consistent within a taxon. Soulié-Märsche (1999), utilising a suite of characters that are useful in palaeobotany, found that oospores were useful for separating closely related, but morphologically and genetically distinct, species (as determined through breeding studies; Proctor et al. 1971). It is probable that taxa with different oospores are genetically incompatible. The genus Chara The name Chara was originally given to four species of ‘little horse-tail’ (Equisetum sub aqua repens) by Linnaeus (1853) in his Species Plantarum (Wood 1965; Moore 1986), and was eventually redefined to include more species, and exclude the genera Nitella (Agardh 1824), Lychnothamnus (Ruprecht 1845) and Tolypellopsis (von Leonhardi 1863) (= Nitellopsis Hy). The genus Lamprothamnus (Braun and Nordstedt 1882) (= Lamprothamnium Groves (1916)) was erected to take C. alopecuroides, C. papulosa, C. wallrothii and C. barbata (= Lychnothamnus barbatus Leonhardi) and Womersley and Ophel (1947) placed two Australian species in Protochara. Several other generic names have been proposed for different parts of the genus (e.g. Charopsis Ruprecht), because it has been recognised that the variation in vegetative morphology

An overview of Chara L. in Australia


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Table 1. Currently accepted species of Chara described for Australia Taxon

Synonymous taxa (Wood 1972)

A

C. contraria A. Braun ex Kütz. A,B C. contraria var. behriana A. Braun C. foetida A. Braun A,B C. contraria var. australis A. Braun C. fragilis Desvaux A C. leptosperma A. Braun A C. virgata Kütz. C. brachypus A. Braun C. gymnopus A. Braun A,B C. australis R. Br. A,B C. australis var. lucida A. Braun B C. australis subsp. estipulodica Macdonald and Hotchkiss BC. australis var. nobilis A. Braun C. australis var. vieillardii Zaneveld A,B C. australis f. simplicissima (Filarszky) R.D. Wood A,B C. inflata (Filarszky) Macdonald and Hotchkiss B N. stuartiana Müll. ex. Kütz. B C. plebeja A. Braun B Protochara australis Wom. et Ophel C. coronata Ziz ex. Bischoff A,B C. muelleri (A. Braun) A. Braun A,B C. leptopitys subsp. subebracteata Nordstedt A,B C. mollusca A. Braun ex. Kütz.

Chara vulgaris L. C. vulgaris var. gymnophylla (A. Braun) Nym.

A

Chara globularis Thuill. em. R.D.W. (3 forms) C. globularis var. virgata (Kütz.) R.D. Wood C. globularis var. leptosperma (A. Braun) R.D. Wood A Chara setosa Kl. ex. Willd. A Chara zeylandica Kl. ex. Willd Chara corallina Kl. ex. Willd. B C. corallina var. nobilis (A. Braun) R.D. Wood (4 forms)

Chara braunii Gmelin Chara baueri A. Braun em. R.D. Wood A,B Chara leptopitys A. Braun Chara ecklonii A. Braun em. R.D. Wood B Chara ecklonii var. mollusca (A. Braun ex. Kütz) R.D. Wood A,B Chara ecklonii var. albaniensis R.D. Wood Chara fibrosa Ag. ex. Bruz., em R.D. Wood (20 forms) B C. fibrosa var. hookeri (A. Braun) R.D. Wood (two forms) B C. fibrosa var. myriophylla (A. Braun) R.D. Wood

A

C. dichopitys A. Braun A,B C. drumondii A. Braun A,B C. arhnemensis (R.D. Wood) R.D. Wood C. benthamii A. Braun C. flaccida A. Braun A,B C. fibrosa var. acanthopitys A. Braun C. gymnopitys A. Braun A,B C. hookeri A. Braun A,B C. microphylla F. Muell. ex Kütz. A,B C. myriophylla F. Muell. ex A. Braun A,B C. preissii A. Braun A,B C. submollusca Nordstedt A,B C. subtilis Kütz. A,B C. tylacantha Nordtstedt C. hydropitys Reich.

Previously described taxa that may be retained or reinstated for Australia in the future; B Australian endemic taxon.

within the genus Chara can be greater than that among genera. The current definition of Chara, outlined in Wood (1965), but developed and clarified by several of his predecessors, is based on the arrangement of gametangia, arising from a single peripheral nodal cell, with the oogonium above the antheridium, where they occur together. Vegetative characters that occur with this are the presence of stipulodes below the branchlet whorls, the frequent occurrence of cortication on the axis and branchlets, monopodial branchlets with bract-cells at the branchlet nodes, and bracteoles arising from the gametangial stalk (Wood 1965). During the 1800s, Chara was divided into ‘logical’ subdivisions (e.g. Haplostephanae, Diplostephanae), which were

developed and used by Braun and Nordstedt (1882) to organise the first world monograph of the group. Wood’s (1965) subdivision of Chara into subgenera, sections and subsections following the International code of botanical nomenclature was based on Braun’s divisions (Braun and Nordstedt 1882; Wood 1965; Proctor 1980). As a consequence the genus was divided into subgenera and then into sections Chara, Desvauxia, Grovesia, Charopsis and Agardhia, of which all have representatives in Australia except Desvauxia. Each section was divided into subsections, and the arrangement of species within these is subject to question on biogeographic (Proctor 1980) and genetic grounds (McCourt et al. 1999). It is of some value to consider

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Table 2. Character states for Chara species in Australia Coded data are in parentheses. Characters 1–11 were used by Wood (1972) to determine subgenera, sections, subsections and species. Characters 12–16 have been shown to be indicative of breeding incompatibility in at least some sections and subsections of Chara (Proctor 1975), and characters 17–24 are hypothesised here to have value in species determination. Characters 22–24 have been used in species determination of fossil charophytes Character for Chara 1. Number of tiers of stipulodes 2. Ratio of number of cortical cells and branchlets

3. Branchlet cortication

4.Character of the basal branchlet segment

5. Spine cells

6. Character of the branchlet tips

7. Ratio of number of stipulodes and branchlets

8. Spine cell, stipulode, bract cell, bracteole length

9. Stipulode, bract cell, bracteole diameter 10. Degree of incrustation 11. Oospore colour 12. Sexual state

13. Number of shield cells on the antheridium 14. Number of chromosomes

15. Placement of spine cells

16. Distribution

17. Placement of gametangia

18. Arrangement of gametangia

19. Degree of development of internal and external bract-cells

Character state Single tier (0) Two tiers (1) 0x (0) 1x (1) 2x (2) 3x (3) Absent (0) Partial (1) Present (2) Naked (0) Corticated (1) Diaphanous (2) None (0) Solitary (1) Fasciculate (2) Single cell (0) Single cell with bract cells (1) Three equal sized cells (2) 1x (0) 2x (1) 3x (2) Absent (0) Shorter than axis (1) Longer than axis (2) Normal (0) Inflated (1) Non-calcified (0) Calcified (1) Black (0) Brown (1) Dioecious (0) Monoecious conjoined (1) Monoecious sejoined (2) 4 (0) 8 (1) 14 (0) 28 (1) 42 (2) All cortical cells the same (isostichous) (0) Spine cells on primary cortical cells (tylacanthous) (1) Spine cells on secondary cortical cells (aulacanthus) (2) Tasmania (0) Mainland Australia (1) Australia and other continents (2) Foliar (0) Internal to the base (1) External to the base (2) Singular (0) In 2s (geminate) (1) More than 2s (clustered) (2) None (0) Verticillate (1) Internal larger (2)



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Table 2. continued Character for Chara

Character state

20. Shape of coronula cells

Round (0) Oval (1) Attenuate (2) Appressed (3) 100–200 (0) 300–400 (1) 500–600 (2) 700–800 (3) 900–1000 (4) Round (0) Oval (1) Cylindrical (2) Rectangular (3) Ovate (4) Obovate (5) < 5 (0) 5–8 (1) 9–11 (2) 12–15 (3) > 16 (4) Granulate (0) Porate (1) Reticulate (2) Fibrous (3) Smooth (4) 200–300 (0) 400–500 (1) 600–800 (2) > 1000 (3)

21. Oospore length in µm

22. Oospore shape in side view

23. Oospore striae

24. Oospore ornamentation

25. Diameter of antheridia in µm

these groupings when working on charophyte taxonomy, but only when the groups have phylogenetic integrity. Determining the phylogeny of charophytes is currently a field of active research (e.g. Karol et al. 2001) and the next few years are likely to see several significant publications concerning this. The aim of this study was to discuss the systematics of Australian charophytes from an historical perspective and in relation to modern species concepts, use oospore morphology to illustrate variability within the genus Chara, as well as to outline an approach to creating a reliable taxonomy for the group. Materials and methods About 400 specimens of Chara in the National Herbaria of Victoria, Tasmania, South Australia and Western Australia and the personal collection of the author were examined to compile a database of specimens and their characteristics. Only good, fertile specimens on which antheridia, oogonia and oospores were available were used in this study. Specimens of all the Chara species listed in Wood (1972) were examined, except for C. setosa Kl. ex Willd., an apparently rare species occurring in tropical Australia and Asia, which was not present in the collections examined. Specimens were each allocated a workbook page number (pXXX) for consistent referencing. Overall morphology was examined with dissecting and high power Zeiss microscopes

(Carl Zeiss International, Göttingen, Germany) and the results were entered into a database. Using table 2 in McCourt et al. (1996) as a model, the characters (and character states) used by Wood to determine species were assembled from Wood’s (1965, 1972) treatments (Table 2, characters 1–11). The characters that have been shown to be uniformly indicative of speciation (breeding incompatibility) by Proctor et al. (summarised in Proctor 1975) were also listed, and another nine characters that could be informative were included (Table 2). Those last nine characters (17–25) were derived from observation of specimens, reference to taxonomic literature other than Wood (1965) (i.e. Braun and Nordstedt 1882; Nordstedt 1891; Groves and Allen 1935; van Raam 1995) and discussion with other taxonomists, and must be considered hypothetical until they are shown via experimentation to be indicative of breeding incompatibility. Characters 21–23 have been used in the study of fossil charophytes for determination of species (Grambast 1974) and are increasingly found to be important in species determination of extant species (e.g. John et al. 1990; Soulié-Märsche 1999). The character states were then determined for each of Australian species of Chara (Wood 1972), based on the literature and direct measurements of Australian specimens referred to above and entered into a data matrix (Table 3). Oospores were prepared for scanning electron microscopy by manual or chemical cleaning (following modifications of the methods by Casanova 1991 or Crawford et al. 2001), mounted on stubs with carbon sticky tabs, coated with gold and viewed with a Phillips XL-30 field emission scanning electron microscope (Phillips, Eindhoven, The Netherlands) operated at 2 kV. Chromosome counts were made by the methods outlined in Casanova (1997).

C. vulgaris C. globularis C. setosa C. zeylandica C. corallina C. braunii C. fibrosa C. ecklonii C. leptopitys C. baueri

Species 1 1 1 1 0 0 0 0 0 0

1 2 3 3 3 0 0 123 12 23 23

2 012 2 2 2 0 0 01 0 0 0

3 1 1 2 0 0 0 0 0 0 0

4 1 01 1 1 0 0 12 12 1 1

5 0 0 0 0 01 2 1 1 1 2

6 1 1 1 1 01 0 012 0 01 0

7 012 01 12 12 01 2 12 2 1 12

8 0 0 0 0 01 0 0 1 0 01

9 1 1 1 1 01 01 01 0 0 01

10 0 01 0 0 0 0 01 0 0 0

11 1 1∗ ?∗ 0∗ 1∗ 1∗ 1∗ 1∗ 1∗ 1∗

∗

1 012∗ 1∗ ?∗ 02∗ 1∗ 012∗ ?∗ 012∗ 2∗

∗

012 0∗ ?∗ 0∗ – – 012∗ 0∗ 01∗ –

∗

02 02∗ 2∗ 2∗ 02∗ 2∗ 02∗ 02∗ 01∗ 2∗

∗

Character (codes in Table 2) 13∗ 14∗ 15∗ 16∗

1 1∗ 1∗ 1∗ 012∗ 1∗ 012∗ 0∗ 0∗ 1∗

∗

12∗ 0 0 0 0 012 0 0 01 012 0

17 0 01 0 0 012 01 01 0 012 01

18

12 2 2 12 02 12 1 2 1 12

19

23 13 ? 2 0123 2 123 2 2 2

20

12 123 23 1234 1234 123 01234 12 12 123

21

12 12 1 1 13 1 0145 1 1 1

22

234 23 3 23 01 123 123 12 1 12

23

04 04 ? 01 04 04 0134 01 01 02

24

012 01 01 01 023 01 012 1 123 0

25

Table 3. Characters for species of Chara in Australia (taken from Wood (1972, 1965) and observations on approximately 400 specimens Characters 1–11 were those used by Wood (1972), characters 12–16 (∗ ) have been shown to be indicative of breeding incompatibility (Proctor 1975) and characters 17–26 are hypothesised here to be indicative of breeding incompatibility. Characters 22–24 are used in determination of fossil species. More than one number indicates more than one character-state in specimens. A dash indicates the character is not assessable. ? indicates that information is not available

30 Australian Systematic Botany M. T. Casanova



Results When species are listed in relation to those characters that Wood used for determination, they show relatively few polymorphisms (Table 3, characters 1–11). However, when those taxa are examined in relation to the characters that have been shown to be indicative of breeding incompatibility (Table 3, characters 12–16) the variability within Wood’s ‘species’ concepts becomes apparent. Character 16 (distribution) indicates that all of the taxa are distributed on more than one continent, except C. leptopitys, which occurs on the Australian mainland and on Tasmania. Proctor (1975) wrote that ‘Suggestions of conspecificity between populations from isolated land masses . . . should be viewed

a

with scepticism unless supported by experimental data . . .’. The additional nine characters (17–25) have little (e.g. John et al. 1990; Casanova 1997; Soulié-Märsche 1999) or no experimental support for their taxonomic value, but have been widely used to support species determinations, and these also display a greater degree of polymorphisms than Wood’s characters. In relation to these results and the variation in oospore characters (Figs 1–19), the status of each Australian species (sensu Wood 1972) is outlined below within their sections.

a

b

b

Fig. 1. (a) Oospore (minus gyrogonite) of specimen p244 Chara contraria var. australis (= C. vulgaris var. vulgaris sensu RD Wood) from Port Fairy, Victoria [M.T. Casanova p244; author’s collection] with 15–16 low striae, (scale bar = 200 µm), (b) oospore wall appears rugulose (scale bar = 2 µm).

a

31

Fig. 3. (a) Oospore (minus gyrogonite) of specimen p630 Chara sp. from coastal Lake Monibeong in western Victoria [T. Dugdale 2004; author’s collection] with 17 strong ridges on the striae (= C. vulgaris var. vulgaris sensu RD Wood) (scale bar = 200 µm), (b) oospore wall is finely granulate (scale bar = 2 µm).

a

b

b

Fig. 2. (a) Oospore (minus gyrogonite) of specimen p041 Chara contraria var. behriana (= C. vulgaris var. gymnophylla sensu RD Wood) from Spear Creek in the Southern Flinders Ranges SA [R. Grandison 1986; MEL] with 13–14 low striae, the oospore has been cracked during cleaning (scale bar = 200 µm), (b) oospore wall is finely granulate (scale bar = 2 µm).

Fig. 4. (a) Oospore (minus gyrogonite) of specimen p658 Chara sp. from Hammersley Gorge, Western Australia [MT Casanova 2004; author’s collection] with flanges on the nine striae (partly removed in cleaning) and no ‘cage’ at the base of the oospore (= C. globularis var. globularis sensu RD Wood) (scale bar = 200 µm), (b) oospore wall is roughened (scale bar = 2 µm).

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a

b

a

b

Fig. 7. (a) Oospore (minus gyrogonite) of specimen p649 Chara zeylandica var. humboltiana from the Pilbara region of Western Australia [MN Lyons & DA Mickle 3076] with 10–11 striae and evidence of a flange or ‘ribbon’ (sensu John et al. 1990) (scale bar = 200 µm), (b) oospore wall is granulate (scale bar = 2 µm).

Fig. 5. (a) Oospore (minus gyrogonite) of Chara globularis var. globularis, Jimberlana Station, Western Australia [B. Archer 1607; MEL] with a ‘cage’ at the base of the oospore (scale bar = 200 µm), (b) oospore wall is smooth (scale bar = 2 µm).

a

a

b

b

Fig. 6. (a) Oospore (minus gyrogonite) of specimen p648 Chara zeylandica var. zeylandica from the Pilbara region of Western Australia [MN & s.d. Lyons 3015, 2003] 10–11 ridged striae (scale bar = 200 µm), (b) oospore wall is highly textured, with light and dark granules (scale bar = 2 µm).

Section Chara According to Wood (1972), in Australia, section Chara contains only Chara vulgaris L., em R.D. Wood, defined as those specimens with 2× cortication on the axis, corticated branchlets and two rows of stipulodes. This is one of the taxa in which Wood saw ‘a continuum of variation, the characters apparently occurring in all possible combinations’ (Wood 1965). Wood’s major change in this group was to unite C. contraria (with spine cells on the primary cortical cells: tylacanthous) and C. vulgaris (with spine cells on the secondary cortical cells: aulacanthous). Subsequent

Fig. 8. (a) Oospore of specimen p036 Chara australis from Warrandyte, Victoria [JD van Bockel & P Coupar 1994; MEL] with 5–6 low striae (= Chara corallina sensu RD Wood) (scale bar = 200 µm), (b) oospore wall is smooth to slightly roughened (scale bar = 2 µm).

experiments (Grant and Proctor 1971) have shown that the two species are distinct, although they cannot always be determined from preserved material. Representatives conforming to both C. vulgaris and C. contraria have been found in Australia. Some Australian specimens have naked, or only partly corticated branchlets, and the second row of stipulodes is often obscure. Braun (1852) described two taxa for Australia C. contraria var. australis (Fig. 1) and var. behriana (Fig. 2) that Wood incorporated into C. vulgaris var. vulgaris and var. gymnophylla. Grant and Proctor (1971) found that ecorticate and corticate clones of C. vulgaris were reproductively isolated. Some specimens have significantly different oospores (Fig. 3) with 17–19 striae, more than has been recorded for any other


a


b

a

Fig. 9. (a) Oospore of specimen p672 Chara sp. from the Pilbara region of Western Australia [MN Lyons & DA Mickle 3070 B] with five thick striae (‘pachygyra’) (= Chara corallina var. nobilis sensu RD Wood) (scale bar = 200 µm), (b) oospore wall is smooth to slightly roughened (scale bar = 2 µm).

a

33

b

Fig. 11. (a) Oospore of specimen p204 Chara sp. from Swan Hill, Victoria [RD Wood 1961; AD] with eight strongly flanged striae (= C. baueri form muelleri det. RD Wood) (scale bar = 200 µm), (b) oospore wall is roughened and pitted (scale bar = 2 µm).

b a

Fig. 10. (a) Oospore of specimen p061 Chara muelleri from South Australia [Mueller 1848; MEL] with 10 low striae (= C. baueri form muelleri det. RD Wood) (scale bar = 200 µm), (b) oospore wall is smooth (scale = bar 2 µm).

charophyte (Wood 1959). The status of the two Australian varieties in this group (vars australis and behriana) needs examination. The variation in oospores in this group found so far (Figs 1–3) indicates that there is more than one, and possibly three, good species in Australia, one of which awaits description. Section Grovesia Wood’s (1965) section Grovesia included subsections Grovesia, Küetzingia and Willdenowia. All species in the section have 3× corticated axes, corticated branchlets and two rows of stipulodes: Chara globularis in subsection Grovesia is characterised by globular stipulodes, straight branchlets and normal basal branchlet cortex. Wood retained three varieties in C. globularis: vars globularis, virgata and leptosperma (Wood 1972). Most of the Australian specimens

b

Fig. 12. (a) Oospore of specimen p529 Chara mollusca from Lake St Clair, Tasmania [T. Dugdale 2004; author’s collection] with approximately eight indented, inconspicuous striae (= C. ecklonii var. mollusca sensu RD Wood) (scale bar = 200 µm), (b) oospore wall is smooth to roughened (scale bar = 2 µm).

examined (approximately 40) conform to the type variety and have oospores with the distinctive ‘basal cage’ typical of var. globularis (Fig. 5). However, Australian collections also contain specimens with long bract-cells and bracteoles, and others with unusual pigmentation, oogonia, gyrogonites and oospores (Fig. 4). Proctor’s (1971) experiments with C. globularis sensu Wood showed that the varieties were reproductively isolated, and should be recognised at the species level. Chara setosa in subsection Kützingia differs from C. globularis in the character (colour and type) of cortication on the basal branchlet segment. Wood included this species in the Australian treatment on the basis of a few records

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a


M. T. Casanova

b

Fig. 13. (a) Oospore of specimen p669 Chara ecklonii var. albaniensis from the Pilbara region of Western Australia [MN Lyons & DA Mickle 3019 B] with six thick ridges on the striae (‘pachygyra’) (scale bar = 200 µm), (b) oospore wall has low, smooth verrucae (scale bar = 2 µm).

a

Fig. 16. (a) Oospore of specimen p335 Chara sp. from the Fleurieu Peninsula, South Australia [RD Wood & HBS Womersley 1961; AD] with eight low ridges on the striae (= Chara fibrosa var. fibrosa form fibrosa det. RD Wood) (scale bar = 200 µm), (b) oospore wall is very finely granulate (scale bar = 2 µm).

a a

b

b

Fig. 14. (a) Oospore of specimen p576 Chara leptopitys from Tasmania [T. Dugdale 2004; author’s collection] with 8–9 low ridges on the striae (scale bar = 200 µm), (b) oospore wall is smooth to roughened (scale bar = 5 µm).

a

b

b

Fig. 15. (a) Oospore of specimen p642 Chara sp. from the Pilbara region of Western Australia [MN Lyons & DA Mickle 3025] with 7–8 strong flanges on the striae (= C. leptopitys sensu RD Wood) (scale bar = 200 µm), (b) oospore wall has low verrucae (scale bar = 2 µm).

Fig. 17. (a) Oospore of specimen p631 Chara fibrosa var. fibrosa form acanthopitys sensu RD Wood from Lake Monibeong, Victoria [T. Dugdale 2004; authors collection] with eight inconspicuous striae (scale bar = 200 µm), (b) oospore wall is smooth and cracked (scale bar = 2 µm).

from the Northern Territory. It is probably under-collected in Australia, and no specimens were seen in this study. Subsection Willdenowia contained just Chara zeylandica worldwide, according to Wood (1972), and he allocated Australian specimens to the type subspecies, variety and form. Several different species are recognised by other authors (Robinson 1906; McCracken et al. 1966). It is likely that this species has been under-collected in Australia, since its habitat requirements seem to coincide with those of crocodiles. The number of specimens examined in this study (approximately 12, e.g. Figs 6, 7), while exhibiting some morphological and oospore variation, are too few to challenge Wood’s estimation of a single species for Australia. On the basis of the results of breeding studies on these taxa overseas


a


b

Fig. 18. (a) Oospore of specimen p628 Chara fibrosa var. hookeri sensu RD Wood from Lake Edward, South Australia [T. Dugdale 2004; authors collection] with eight indented striae (scale bar = 200 µm), (b) oospore wall is smooth and cracked (scale bar = 2 µm).

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is the cortication on the main axis (a late developing character in C. muelleri), a thorough study of these taxa is required. In Wood’s (1972) revision of Australian Characeae, he amalgamated endemic dioecious C. australis vars australis (Fig. 8), lucida and nobilis (Fig. 9), C. australis subspecies estipulodica, N. stuartiana, C. plebja, and Protochara inflata with monoecious C. corallina, but distinguished varieties corallina and nobilis with the recognition that var. corallina was consistently dioecious in Australia (in contrast to the rest of its range through Asia), and that var. nobilis could be separated into four forms: nobilis, stuartiana, simplicissima and inflata (Wood 1972). Current research into this group (Garc´ıa and Casanova unpublished data) indicates that many of the taxa that were described previously will be reinstated, resulting in several species within this group. Section Agardhia

a

b

Fig. 19. (a) Oospore of specimen p056 Chara fibrosa var. fibrosa form arnhemensis from Arnhem Land, Northern Territory [Specht 1948; MEL] with eight low ridges on the striae (specimen distorted and cracked in cleaning) (scale bar = 200 µm), (b) oospore wall is spongy and porate (scale bar = 2 µm).

(Proctor 1971) it is likely that section Grovesia contains at least five, and possibly six, good species in Australia. Section Charopsis The name Charopsis was originally given at genus level to encompass ecorticate species, excluding those in Nitella, Lamprothamnium and Lychnothamnus (Ruprecht 1845). Wood retained this name for a subgenus and section in Chara. This section contains a diverse range of taxa in Australia. Wood (1965) placed C. corallina (distributed through Asia, Australia and the Pacific), C. socotrensis (restricted to India, Burma, Indonesia and Socotra Island) and C. braunii (world wide) in the section. However, genetic analysis indicates that C. braunii is not closely related to the other taxa in the section, and more closely related to C. muelleri (Meiers et al. 1999). Wood thought that the Australian examples of C. braunii were few and poor, and I have seen only a few specimens I would definitively identify as C. braunii. Given the similarity of C. braunii and C. muelleri, and the fact that the only consistent difference between them

The situation is even more complicated with section Agardhia. Wood’s (1972) section Agardhia was divided into subsections Agardhia, Braunia and Wallmania, of which Agardhia and Braunia occur in Australia. Braunia consists of C. baueri from Europe and Kazakhstan (Langangen and Sviridenko 1995), which Wood amalgamated with C. muelleri from Australia. These taxa are similar (differing in the presence of spine cells, posterior bract-cells and size of the oospores; Nordstedt 1891), but given their disjunct distribution, and the intercontinental genetic isolation within the genus, it is likely that C. muelleri will be found to be a separate species. Nordstedt (1891) followed Braun’s treatment, but felt that C. muelleri ‘ought perhaps be regarded as a separate species’. Within the broad description of C. muelleri in Australia there is a large degree of variation in vegetative morphology and oospore features (e.g. Figs 10, 11, cf. Casanova 1997), so further revision of this taxon is needed. Subsection Agardhia in Australia contains C. fibrosa, C. leptopitys and C. ecklonii (Wood 1972). Woods concept of C. leptopitys included all taxa in subsection Agardhia with basal gametangia, and included Nordstedt’s (1891) subspecies subebracteata as a form. There is some variation in C. leptopitys, with apparently distinct entities in Tasmania (Fig. 14), Western Australia (Fig. 15) and Victoria, and if gametangial arrangement is diagnostic of species differences (Proctor 1975) then the arid zone taxon subebracteata should also be considered separate at the species level because this is the only taxon in Chara in which gametangia are clustered outside the base of the whorl (cf. Lamprothamnium in which at least two species have this arrangement). The variation in C. leptopitys is also apparent in the oospores (Figs 14, 15). Chara ecklonii (as amended by Wood) was the product of amalgamating endemic Tasmanian C. mollusca (Fig. 12) and African C. ecklonii (Wood 1965), maintaining the

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Tasmanian material as a separate variety. Wood (1972) added C. ecklonii var. albaniensis (Fig. 13) on the basis of a single incomplete male specimen collected in Albany, WA (Wood 1972). It is possible that C. ecklonii in southern Africa and var. albaniensis in southern Western Australia are related, since there are common elements in the vascular flora of the two regions (e.g. family Proteaceae). However, given the disjunct distribution and intercontinental genetic isolation in similar disjunct entities (Proctor 1975), it seems unlikely that they are the same species. Chara fibrosa is a huge taxon. Wood’s first efforts followed those of Zaneveld (1940) quite closely in lumping C. gymnopitys and C. fibrosa, but by the time he was working on the Australian specimens he saw fit to amalgamate at least 15 species that were described previously into C. fibrosa. Within that he was able to distinguish three varieties: var. fibrosa (with 20 forms, e.g. Figs 16, 17, 19; cf. Casanova 1997), var. hookeri (two forms e.g. Fig. 18) and var. myriophylla in Australia (Wood 1972). The variation in vegetative morphology among these entities is large, and there are correspondingly large differences in the oospores (Casanova 1997; Figs 16–19). Initial analyses indicate there are between six and 20 good species in this group (MT Casanova, A Garc´ıa unpubl. data). Discussion This examination of Wood’s taxonomy indicates that there are more than 10 taxa of Chara in Australia. As indicated by A in Table 1, there are 35 taxa that have been described previously. Based on the level of separation among currently accepted species, it is likely that these taxa are different species, and that they will be shown to be genetically incompatible. van Raam restored some of Wood’s varieties to species in his review of Tasmanian charophytes (van Raam 1995), specifically C. hookeri A. Braun, C. myriophylla A. Braun, C. preissii A. Braun and C. contraria A. Braun ex. Kütz. It is probable that this will also be done for the same taxa where they occur in other states (e.g. Garc´ıa 1999). Some of Wood’s amalgamated taxa are probably different species from those that occur on other continents or in the northern hemisphere. When overseas specimens are examined some of these are clearly morphologically distinct from Australian specimens. In studies where charophytes from different continents were crossed, Proctor (1971) found that they were invariably incompatible, and that the likelihood that such entities would be inter-fertile was low. Where such groups are being revised it will be necessary to include overseas specimens in the analyses to determine whether there is sufficient overlap for these broader species to be retained. Some specimens stand out as distinctly different taxa, possibly undescribed species (e.g. p630 Fig. 3). However, much of the diversity in Australian charophytes has already been described (e.g. C. preissii, C. hookeri,

M. T. Casanova

C. myriophylla, and so on, Table 1) and examination of the original descriptions will be required to allocate names to the groups. Do the taxa in Wood’s concept of Chara represent more than one genus? The evidence from morphological and genetic analysis (Garc´ıa and Karol 2004) suggest that at least one species has been misplaced in Chara. The variation in vegetative morphology in the group is huge, ranging from totally corticate taxa with ‘all the optional extras’, to ‘stripped down’ taxa with few taxonomic characters apart from gametangial features and cell dimensions. Despite this, genetic analyses (McCourt et al. 1999; Meiers et al. 1999) support monophyly in the genus. The status of Protochara as a separate genus has not been supported by either breeding studies (Macdonald and Hotchkiss 1956) or more recent analysis (Garc´ıa and Karol 2004). Separating Wood’s subgenera (Chara and Charopsis) or sections (Chara, Grovesia, Charopsis and Agardhia) could be justified if there was some agreement on the level of genetic divergence at the level of ‘genus’ in other algal or vascular plant groups. The question could well be irrelevant in the future if recent initiatives involving the Phylocode (Cantino and de Queiroz 2004) become generally accepted. Once we recognise that we have an unusable taxonomy at species level, what can we do about it? Wood reduced previously described species to varieties and forms. Can’t we just use Wood’s varieties and forms to recognise the diversity? Unfortunately, we cannot. In many cases he amalgamated dioecious taxa with monoecious ones, and did not preserve the dioecious taxon name at any level (e.g. Chara preissii, Nitella sonderi). In many cases Wood’s forms do not equate with any previously recognised taxon and are not named (e.g. 15 of the 20 forms in C. fibrosa var. fibrosa). This is in addition to the fact that the nomenclature is clumsy, and the temptation to simply use the specific epithet (rather than variety and form) reduces the value of the classification. Can’t we use a previous treatment? The only other published works on reasonable numbers of Australian charophytes are Braun and Nordstedt (1882, mostly in German), Nordstedt (1918), Groves and Allen (1935) for the Queensland charophytes and, more recently, van Raam (1995) for Tasmanian charophytes. All of these overseas workers depended on preserved specimens, and usually few fertile collections, so their descriptions might not contain the range of characteristics in the species. In some cases a species has been erected on the basis of a single collection (e.g. Nitella tumida, Nordst. N. partita, Norsdst.), and some of these have not, or have rarely been collected since the original collection, thus the authors were not able to examine the range of variation within the taxon. If the specimen was not mature at the time of collection the important oospore characters remain undescribed. None of these authors had access to


scanning electron microscopy, so even if specimens were fertile, oospore characters were not always well described. Many of the species described in the past are good, but the variation within species is not well documented. As well, many areas of Australia were not well sampled for charophytes, and new taxa have been found since these treatments were published. The outstanding exception to most previous Australian studies is that by Williams (Chambers and Williams 1959; Williams 1959). A large number of specimens from a range of sites were examined, and were cultured and grown under controlled conditions to assess the effect of environment on morphology. The oospores were examined in detail and chromosome counts were made. The difference was, of course, that Williams was working in Australia, on fresh material, used all the analytical and technical tools available at the time, and published on one taxon in detail. The early charophyte workers knew they needed more familiarity with specimens to undertake a proper taxonomic analysis [e.g. Nordstedt (1891) in reference to C. leptopitys subspecies subebracteata: ‘The real affinity of these forms can only be ascertained by the examination of a larger number of living specimens, from different localities, and in various stages of growth’ and: ‘the Australian specimens of Characeae . . . are for the most part badly preserved’]. We now have multivariate analytical techniques, scanning electron microscopy and genetic analysis as well as techniques for chromosome counts, culture facilities, and hindsight. We should be able to do at least as good a job now as has been done in the past. The real work in charophyte systematics will be in determining which characters are indicative of breeding incompatibility (and therefore speciation), teasing out the variation and allocating names. Several questions are being answered along the way. How variable is the morphology of species? The culture studies on which Wood relied (e.g. Corillion 1957) did show that some characters (such as arrangement of gametangia and development of cortex) could be modified by nutrient stress. In contrast Proctor (1975) reports that the morphology of individual clones of a large number of species was stable under culture. More recent work by Proctor has shown that charophytes can respond to the presence of grazers by altering the length of spinecells, stipulodes, bract cells and terminal internodes (Proctor 1996). To what extent does this occur in the field? What is in the ‘normal’ range of variation for a species? For taxonomy we would like some discrete morphological variables for species determination, but it might be that probability ranges for continuous variables are going to be more useful. Gene sequences hold great potential for distinguishing between different taxa (e.g. Karol et al. 2001), but how do these relate to breeding compatibility? Oospore morphology is a really important character but no comprehensive study of oospore variation over the whole range of a species has yet been


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undertaken. With so many dioecious species in Australia we should be able to undertake breeding experiments quite easily and therefore determine what level of morphological variance indicates speciation. Studies that include genetic analysis, culture and breeding studies, and analysis of oospore morphology are likely to be rewarding. In general, Northern Hemisphere charophyte experts have not anticipated the amount of variation among Australian charophytes, and have never allocated sufficient time to solve all the problems. They usually indicate this in their texts by mentioning the need for further study (e.g. Wood 1972: 17, 43, 45, 51, 54, 62, 66, 78, 82, and so on; van Raam 1995: 22, 40). What we need now are some thorough, focused studies so that, from a practical point of view, charophyte occurrence and abundance can be used as a predictive and descriptive tool in the management of our water resources. In understanding the variation in charophytes we might also start to understand some of the drivers of biodiversity in Australian inland waters. Acknowledgments Simon Crawford (School of Botany, the University of Melbourne) helped with scanning electron microscopy and oospore cleaning techniques. This ongoing work was initiated by receipt of an ABRS grant to A Garc´ıa and MT Casanova in 2000. Thanks go to numerous collectors from around Australia for sending charophytes. Thanks also go to the staff at the National Herbarium of Victoria for cheerful assistance. Thanks go to Anthony and Robert Casanova for discussion and assistance on collecting trips. I also thank RD Wood for sorting out a huge body of information on Australian charophytes, diligently collecting from hundreds of Australian localities and leaving me something to do. ‘A dwarf standing on a giant’s shoulders can see more than the giant himself’. I thank Vernon Proctor for asking the big questions and encouragement, and two anonymous reviewers for suggestions that have been used to improve this manuscript. References Agardh CA (1824) ‘Systema Algarum.’ (Lundae Literis Berlingianis: Lundae) Braun A (1843) Charae Preissianae adiectis reliquis specibus e nova hollandia hucusque cognitis. Linnaea 17, 113–119. Braun A (1849) Charae australes antarcticae or characters and observations on the Characeae of Australia and the southern circumpolar regions. Hookers Journal of Botany and Kew Garden Miscellany 1, 193–203. Braun A (1852) Characeae. FL von Schlechtendal Plantae Mullerianae. Linnaea 25, 705–709. Braun A, Nordstedt CFO (1882) Fragmente einer Monographie der Characeen. Nach den hinterlassenen Manuscripten. A. Braun’s. Abh. K. Akad. Wiss Berlin 1882, 1–211. Brock MA, Lane JAK (1983) The aquatic macrophyte flora of saline wetlands in Western Australia in relation to salinity and permanence. Hydrobiologia 105, 63–76. doi: 10.1007/BF00025177

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Brock MA, Sheil R (1983) The composition of aquatic communities in saline wetlands in Western Australia. Hydrobiologia 105, 77–84. doi: 10.1007/BF00025178 Brown R (1810) ‘Prodromus florae novae hollandiae et insulare van diemen. Vol. 1.’ (Richard Taylor and Sons: London) Cantino PD, de Queiroz K (2004) http://www.ohiou.edu/phylocode (validated 7 February 2005) Casanova MT (1991) An SEM study of developmental variation in oospore wall ornamentation of three Nitella species in Australia. Phycologia 30, 237–242. Casanova MT (1993) ‘The ecology of Charophytes in temporary and permanent wetlands, an Australian perspective.’ PhD thesis, University of New England, Australia. Casanova MT (1997) Oospore variation in three species of Chara (Charales, Chlorophyta). Phycologia 36, 274–280. Casanova MT (2004a) A census of submerged plants in the Angas River and Tookayerta Creek Catchments. (Report to the River Murray Water Catchment Management Board) Casanova MT (2004b) Charophytes of the Pilbara region of Western Australia. (Report to the Western Australian Department of Conservation and Land Management) Casanova MT, Dugdale TM (2004) Structure and diversity in deep-water charophyte communities in Australia. In ‘Proceedings of the 4th international congress on extant and fossil Charophytes in Robertson (NSW Australia)’. (September–October 2004) Chambers TC, Williams MB (1959) A revision of Nitella cristata Braun (Characeae) and its allies. Part I. Experimental taxonomy. Proceedings of the Linnean Society of New South Wales 84, 338–345. Corillion R (1957) Les Charophycées de France et d’Europe Occidentale. Bull. Soc. Sci. Bretagne 32, 1–259. Crawford SA, Higgins MJ, Mulvaney P, Wetherbee R (2001) Nanostructure of the diatom frustule as revealed by atomic force and scanning electron microscopy. Journal of Phycology 37, 543–554. doi: 10.1046/j.1529-8817.2001.037004543.x Garc´ıa A (1996) Nitella ignescens sp. nov. and N. ungula sp. nov. (Charales Charophyta) from Australia. Phycologia 37, 53–59. Garc´ıa A (1999) Charophyte flora of south-eastern South Australia and south-west Victoria Australia, systematics distribution and ecology. Australian Journal of Botany 47, 407–426. Garc´ıa A, Casanova MT (2004) Lamprothamnium heraldii sp. nov. the first dioecious representative of the genus. Phycologia 42, 622–628. Garc´ıa A, Karol KG (2004) A paradigm in the taxonomy of Charophytes: the oospore and gyrogonite of Nitellopsis inflata (Fil. & G.O. Allen ex Fil.) = Lamprothamnium inflatum comb. nov. In ‘Proceedings of the fourth international congress on extant and fossil Charophytes in Robertson (NSW Australia)’. (September–October 2004) Grambast L (1974) Phylogeny of the Charophyta. Taxon 23, 463–481. Grant MC, Proctor VW (1971) Chara vulgaris and C. contraria: patterns of reproductive isolation for two cosmopolitan species complexes. Evolution; International Journal of Organic Evolution 26, 267–281. Groves J (1916) On the name Lamprothamnus Braun. Journal of Botany 54, 336–337. Groves J, Allen GO (1935) A review of the Queensland Charophyta. Proceedings of the Royal Society of Queensland 46, 34–59. Hotchkiss AT, Imahori K (1988) A new species of Nitella (Characeae) belonging to the pluricellulate species group in Australia. Proceedings of the Linnean Society of New South Wales 110, 175–185. Imahori K, Wood RD (1965) Iconograph of the Characeae. In ‘A Revision of the Characeae. Vol. 2’. (Eds RD Wood, KI Imahori) pp. 1–397. (Cramer: Weinheim)

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Proctor VW, Wiman FH (1971) An experimental approach to the systematics of the monoecious-conjoined members of the genus Chara, series Gymnobasalia. American Journal of Botany 58, 885–893. Robinson CB (1906) The Characeae of North America. Bulletin of the New York Botanical Garden 4, 244–308. Ruprecht FJ (1845) ‘Distributio cryptogramarum vascularium in Imperio Rossico.’ (Beitr. z. Pflanzenkunde d. Russischen Reiches: St Petersburg) Sakayama H, Nozaki H, Kasaki H, Hara Y (2002) Taxonomic reexamination of Nitella (Charales Charophyceae) from Japan based on microscopical studies of oospore wall ornamentation and rbcL gene sequences. Phycologia 41, 397–408. Soulié-Märsche I (1999) Extant gyrogonite populations of Chara zeylandica and Chara haitensis: implications for taxonomy and palaeoecology. Australian Journal of Botany 47, 371–382. van Raam JC (1995) ‘The Characeae of Tasmania.’ (J Cramer: Berlin) Williams MB (1959) A revision of Nitella cristata Braun (Characeae) and its allies. Part II. Taxonomy. Proceedings of the Linnean Society of New South Wales 84, 346–356.

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Womersley HBS, Ophel IL (1947) Protochara, a new genus of Characeae from Western Australia. Transactions of the Royal Society of South Australia 71, 311–317. Wood RD (1959) Gametangial constants of extant Charophyta for use in micropaleo-botany. Journal of Paleobotany 33, 186–194. Wood RD (1965) ‘Monograph of the Characeae. Vol. 1.’ In ‘A revision of the Characeae’. (Eds RD Wood, KI Imahori) pp. 1–904. (Cramer: Weinheim) Wood RD (1972) ‘Characeae of Australia.’ (Cramer: Lehre) Wood RD, Imahori KI (1965) ‘A revision of the Characeae.’ (Cramer: Weinheim) Wood RD, Mason R (1977) Characeae of New Zealand. New Zealand Journal of Botany 15, 87–180. Wood RD, Williams MB (1967) Australian Characeae which survived the Armidale fire. Muelleria 1, 175–196. Zaneveld JS (1940) The Charophyta of Malaysia and adjacent countries. Blumea 4, 1–224.

Manuscript received 23 July 2003, accepted 7 February 2005

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