A revision of Chara sect. Charopsis (Characeae: Charophyceae) in ...

SPECIAL ISSUE CSIRO PUBLISHING

Australian Systematic Botany, 2014, 27, 403–414 http://dx.doi.org/10.1071/SB14032

A revision of Chara sect. Charopsis (Characeae: Charophyceae) in Australia, including specimens collected for Bush Blitz Michelle T. Casanova A,B,C A

Royal Botanic Gardens, Melbourne, Birdwood Avenue, South Yarra, Vic. 3141, Australia. Water Research Network, Federation University, Mount Helen, Vic. 3350, Australia. C Present address: 273 Casanova Road, Westmere, Vic. 3351, Australia. Email: [email protected] B

Abstract. Australian species of Chara L. sect. Charopsis (Kütz.) Leonh. are revised. Multivariate analysis supports recognition of four species: Chara braunii C.C.Gmel., C. evanida Casanova, C. karolii Casanova and C. muelleri (A.Braun) F.Muell. These taxa are described and illustrated, and a key is provided. Additional keywords: Chara braunii, C. baueri, C. evanida, C. karolii, C. muelleri. Received 25 September 2014, accepted 3 February 2015, published online 29 June 2015

Introduction Charophytes (macroalgae in family Characeae) grow submerged in wetlands and rivers world-wide (Casanova 2007). They have a relatively simple morphology, consisting of giant, multinucleate cells arranged end on end, interrupted by whorls of laterals of limited growth (branchlets). The branchlets are usually multicellular, and characteristics of the last cell of the branchlet (the end cell) is diagnostic at genus, subgenus, section or species level. In Chara sect. Charopsis R.D.Wood, instead of a single end cell, there is always a cluster of 3–5 equalsized cells. This was recognised as a useful taxonomic character very early on (Braun 1849), and was termed a corona of cells (not to be confused with the coronula or ‘little crown’ of cells at the apex of the oogonium). The family Characeae was revised for Australia by Wood (1971); however, that revision resulted in an unusable taxonomy (Casanova 2005, 2009), and some sections have since been revised (Casanova 2013a; Casanova and Karol 2014). In the present revision, Australian species of Chara sect. Charopsis are examined. Historical review The genus Chara comprises two subgenera, Chara and Charopsis (Kütz.) Leonh., defined on the basis of the number of stipulode whorls at the base of the branchlets (Wood and Imahori 1965; see also Casanova and Karol 2014 for a description and history of subgen. Charopsis). Subgen. Charopsis has three sections, namely, Charopsis, Protochara Casanova & Karol (comprising totally ecorticate species with single end cells on the branchlets, revised by Casanova and Karol 2014) and Agardhia R.D.Wood (comprising species with corticated axes, Journal compilation CSIRO 2015

naked branchlets and a single end segment subtended by bract cells at the branchlet tips; see Casanova 2013b). Sect. Charopsis is characterised by a robust morphology with 8–10 branchlets in a whorl, bract cells shorter than the branchlet segments, a well developed, apiculate or acute coronula on the oogonium, and a cluster of end cells (3–5 almost equal-sized cells) at the branchlet tips. The type species of this section, Chara braunii, was described on the basis of specimens collected by Alexander Braun near Carlsruhe (Karlsruhe) in Germany in 1820 (Gmelin 1826). Braun used the later name Chara coronata Ziz ex A.Braun, nom illeg., when he amalgamated C. braunii with several other species (Braun 1849). Braun’s original concept of this taxon was subsequently expanded to encompass material from India, the Mediterranean, much of northern Europe, north Africa, North America and the Pacific, with numerous additional infraspecific taxa described, these variously treated at the rank of species, variety and form, depending on the concepts of individual authors (Braun 1849, 1867; Allen 1871, 1882; Robinson 1906; Zaneveld 1940; Wood and Imahori 1965; Wood and Mason 1977). The earliest mention of C. braunii in Australia was by Nordstedt (1887) from the Richmond River in northern New South Wales. Von Mueller (1889) gave localities (under C. coronata) in Victoria, Queensland and South Australia (Pidinga, W.Tietkins). Groves and Allen (1934) also recorded a specimen of C. braunii from Pine River in Queensland. Wood and Imahori (1965) did not list any specimens of C. braunii from Australia, whereas Wood (1971) noted that specimens of C. braunii from Australia were ‘few and generally poor’, and that the species was rare in Australia, especially when compared with its appearance and distribution on other continents. The work of www.publish.csiro.au/journals/asb

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Wood and Imahori (1964, 1965) did little to clarify the confusion surrounding this name, as the specimen used to illustrate C. braunii (icon 109, J. & T. Howell) was from North America, and so more likely to represent C. braunii var. schweinitzii rather than C. braunii sens. str. Prior to the 1970s, all treatments of the C. braunii complex were based on a subjective assessment of what constituted a species, variety or form within the Characeae. Proctor (1970) undertook the first objective study of six clones of C. braunii from different localities (USA, Israel, Argentina, Pakistan), and found that there was effective genetic isolation among most of the clones tested. Although cross-bred clones could sometimes produce oospores, few of those oospores germinated to produce fertile offspring. Proctor (1970) concluded that C. braunii was a complex of sibling species, each somewhat morphologically different, and each restricted to a single continent, region or sometimes a single water body. This supports an earlier assessment by Allen (1882) who indicated that in any given locality ‘though thousands of plants be examined they will all be found to exhibit precisely the same character’ (p. 359). Along with C. braunii, two other species are considered to comprise sect. Charopsis, namely, C. baueri A.Braun and C. muelleri (A.Braun) F.Muell. (Meiers et al. 1999; McCourt et al. 2000). Chara baueri was first collected by Gustav Heinrich Bauer in the vicinity of Berlin, Germany, in the 1820s, and C. muelleri was collected in South Australia by Ferdinand von Mueller in 1848. These taxa were initially described as separate species, but variously amalgamated into the same taxon at varietal or form level by subsequent authors (Nordstedt 1883; Wood and Imahori 1965; Wood 1971). Both differ from C. braunii sens. lat. by having a corticated axis. For most authors (who considered the presence or absence of cortication to be taxonomically important at the sectional level), C. baueri and C. muelleri were thought to be more closely related to C. fibrosa than C. braunii (Nordstedt 1883; Wood and Imahori 1965; Wood 1971). However, genetic studies by McCourt et al. (2000), and Meiers et al. (1999) placed both corticated and ecorticate species with a corona of end cells on the branchlet (C. braunii and C. muelleri) sister to each other, indicating a closer relationship to each other than to other members of subgen. Charopsis or any members of sect. Agardhia. Morphology Chara species grow as totally submerged water plants, rooted in the sediment via colourless rhizoids, with a photosynthetic axis in the water column. The axis consists of single-celled internodes and whorls of multicellular, uniaxial branchlets, on which the reproductive structures are borne. The axes look very similar to those of submerged flowering plants, and can be confused with species of Myriophyllum L. Species of sect. Charopsis can have a cortex on their axes (i.e. main stems with a covering of smaller cells), but their branchlets are always ecorticate, with a cluster or ‘corona’ of 3–5 somewhat equal-sized cells at the branchlet tips and a conspicuous crown of acute, apiculate or cuspidate coronula cells on the oogonium. Their persistent reproductive units (oospores) are large (420–820 mm: Braun 1867; Casanova 1997; Hutorowicz 2007), with 7–12 spiral sutures or ridges

M. T. Casanova

(striae). In general, species are annual, and typically found in temporary wetlands, or the temporarily inundated edges of permanent water bodies. All the species known are monoecious; those that develop axial cortical cells have either two or three times the number of cortical cells as there are branchlets at the adjacent node (diplo- or triplostichous), spine cells can be obvious or obscure but are never abundant, stipulodes occur in a single whorl below the branchlet whorl (haplostephanous), usually the same number as the number of branchlets (unistipulate), and bract cells are usually well developed only on the adaxial side (i.e. beside the oogonium). There is also the conspicuous development of bracteoles arising from the basal cell of the oogonium. Species in sect. Charopsis are distinguished from similar species in sect. Agardhia by the presence, in Agardhia species, of verticllate bract cells, and a single end segment (1–2 cells long) at the branchlet tips (although the end segment is often subtended by bract cells). Even accounting for the described species and varieties in this group, there is sufficient vegetative, chromosome and oospore variation for other species to be recognised in this group in Australia. Materials and methods Approximately 75 fresh, pressed and spirit-preserved specimens in Australian and overseas herbaria and several private collections were examined for the present study, including type specimens. Each specimen was allocated a letter–number combination (p###, r###, t### or v###), so that all data obtained from individual specimens (i.e. measurements, photographs, chromosome counts, scanning electron micrographs) can be related back to the specimen. Initial examination involved measurements (size, number) directly from the specimen (e.g. length of branchlets, number of branchlet segments) and with the use of a microscope (e.g. axis and branchlet diameter, number of cortical cells, number and morphology of stipulodes and bract cells, arrangement of gametangia). Oospore features were examined and measured with the aid of light microscopy and scanning electron microscopy. Fresh specimens were obtained in field surveys in all states of Australia, and from culture of seed-bank material in a greenhouse (following the methods of Casanova 2004). In the greenhouse, plastic containers (185 mm 125 mm 50 mm) filled with ~300 g of wetland soil were inundated to a depth of 10–14 cm in large tanks and germinated charophytes examined. When oospores were present, they were removed from the specimens for examination with a scanning electron microscope (SEM); then, plants were gathered and pressed, or preserved in 70% alcohol. If oospores were not present, the plants were either returned to culture to mature, or kept in jars on a windowsill until they matured and oospores were freely released. If antheridia were present, chromosome counts were attempted, following the methods outlined in Casanova (1997). Where possible and appropriate, oospores were removed from the herbarium specimens or obtained as above from live material. Approximately 87% (63) of the specimens examined had oospores. They were prepared for SEM examination by cleaning (if required) with a detergent solution, using a modification of the methods of Crawford et al. (2001).

Chara sect. Charopsis in Australia

Sometimes the enveloping cells were removed by hand, using fine needles. For type specimens, very old material or specimens with a single oospore available for examination, the oospores were handled with great care, with minimal manipulation. Oospores were removed from the stubs after microscopy and are stored in alcohol and deposited with the specimen for possible future examination. Data on each specimen were compiled in a spreadsheet and analysed using multivariate statistics in the programs Minitab (ver.11 Statistical Software, Minitab Solutions, State College, PA, USA) and PATN (ver. 3.12, L. Belbin, Blatant Fabrications Pty Ltd, see http://www.patn.com.au). The data were initially investigated using principal component analysis (correlation matrix). The resulting plot of eigenvectors indicated that up to five eigenvalues would be useful for segregation of the data. The characters that contributed >40% to the weighting on the first five eigenvalues were used as variables in a cluster analysis, and semi-strong hybrid multidimensional scaling ordination. The cluster analysis (matrix produced using the Gower metric, fusion using unweighted pairgroup method with arithmetic mean (UPGMA), b = 0.1) resulted in a dendrogram depicting four major groups, and these groups were plotted on the ordination.


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Results Principal component analysis provided three significant eigenvectors for segregation of the specimens, accounting for 50% of the variability in the data. PC 1 was made up of oospore characteristics (width 0.423; end-cell impression 0.416; length 0.423) and branchlet length (0.334). PC 2 was made up of characters related to gametangia (singular, geminate or clustered: 0.428) and the presence of a cortex (cortical cells: 0.342; spine cells: 0.321). PC 3 was heavily weighted by branchlet characters (number of branchlets: 0.453; number of branchlet cells: 0.594). The addition of a further two eigenvectors accounted for a further 20% of the variability, but with the addition of only stipulode length, plant height and oospore flange size as segregating traits. A dendrogram produced by cluster analysis based on the oospore characters, cortex characters and gametangial characters resulted in four major groups of specimens (Fig. 1). The first split separated a group containing the type material of C. muelleri from all others, the second split separated the remainder of the corticated specimens (except C. baueri) from the ecorticate species, the third split separated two groups of ecorticate specimens, the overseas material of C. braunii (and varieties) was largely nested within one group containing specimens from South Australia and Western Australia, and the final group represented specimens from eastern Australia. Within the species groups identified in the present study (indicated by the different symbols) there were regional groupings that can be identified, which might represent different genetic entities (Fig. 1). Group A represents specimens from the Murray–Darling Basin, Group B represents specimens from wetland systems in northern New South Wales, group C represents specimens of C. braunii from South Australia, group D represents specimens from western Victoria, group E represents C. muelleri from the lower lakes and Fleurieu Peninsula regions of South Australia, and group F represents C. muelleri from the New England Tablelands in New South Wales.

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Fig. 1. Dendrogram based on cluster analysis (Gower metric, unweighted pairgroup method with arithmetic mean, b = 0.1), illustrating similarity of specimens in sect. Charopsis on the basis of cortication, gametangial arrangement and oospore characters. Different symbols represent different species or specimens: C. braunii (Australian material, open inverted triangles); C. braunii (German material, closed squares); C. braunii (USA material, closed circles); C. baueri (closed right-facing triangles); C. evanida (open circles); C. karolii (open squares); C. muelleri (open triangles); and C. muelleri (type material, closed triangles). The groups labelled with different capital letters represent specimens from specific regions in Australia (see text).

An ordination plot of the data in two dimensions (Fig. 2), based on cortex, branchlet and oospore characters, revealed nonoverlapping segregation of the specimens in three of the four major groups (circled) identified by different symbols, with the fourth group and the overseas specimens occurring in-between the groups of Australian specimens. The fourth group is more easily seen in plots against the third dimension. These analyses provided evidence for the segregation of four species on the basis of morphological features. Two of these species have already been described and two are different from all other described species. The four species are described below.

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Chara braunii C.C.Gmel. Fl. bad. 4, 646 (1826)

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Charopsis braunii (C.C.Gmel.) Kütz. Phyc. general. 319 (1843); Nitella braunii (C.C.Gmel.) Rabenh., Deutschl. Krypt.-Fl. 2, 197 (1847).

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Type: ‘Circa Carlesruhe in fossis aquaticis prope Rintheim et Scheibenhart, magna in abundantia vidit acutissimus Alex. Braun, 1820’. Neo: near Oldenico Italy, A. Malinverni s.n. 1856, NY (fide Wood and Imahori 1965, p. 262).

PC axis 1 (22%)

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Chara coronata Ziz ex Bisch., Krypt. Gew. 26, pl. I, fig. 7 (1828). –3

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PC axis 2 (18%) Fig. 2. Ordination of specimens in sect. Charopsis on the basis of cortication, gametangial arrangement and oospore characters. Different symbols represent different species or specimens: C. braunii (Australian material, open inverted triangles); C. braunii (German material, closed squares); C. braunii (USA material, closed circles); C. baueri (closed right-facing triangles); C. evanida (open circles); C. karolii (open squares); C. muelleri (open triangles); and C. muelleri (type material, closed triangles). Three of the four groups identified in the cluster analysis are circled.

Chara L., Sp. Pl. 2, 1156 (1753) Type: Chara vulgaris L. Chara subgen. Charopsis (Kütz.) Leonh., Lotos 13, 73 (1863) Charopsis Kütz., Phycol. General. 319 (1843)

Type: Chara braunii C.C.Gmel. Monoecious or dioecious. Plant axis corticated or ecorticate, stipulodes in a single whorl (haplostephanous), bract cells unilateral or verticillate, branchlets ecorticate and terminated by a single cell, a cluster of bract cells or a group of 3–5 equal-sized cells (corona). Chara subgen. Charopsis (Kütz.) Leonh. sect. Charopsis Chara sect. Heterosiphoniae Wallr., Fl. Crypt. Germ. l07 (1833), p.p. Chara sect. Monosiphoniae Wallr., Fl. Crypt. Germ. l07 (1833), p.p. Chara a. Ecorticatae A.Braun Hooker’s J. Bot. 1, 294 (1849), p.p. Chara subsect. Ecorticatae (A.Braun) Leonh. Lotos 13, 73 (1863), p.p. Chara subsect. Braunia R.D.Wood, Taxon 11, 14 (1962).

Monoecious with an annual life-history. Plant axis corticated or ecorticate, sometimes cortex restricted to the upper internodes, stipulodes in a single whorl (haplostephanous), bract cells adaxial, unilateral, branchlets ecorticate and terminated by a group of 3–5 equal-sized cells (corona). Coronula cells acute or apiculate. Key to species of sect. Charopsis in Australia 1. Plants ecorticate throughout....................................................................2 Plants with corticated axes......................................................................3 2. Bract cells well developed at fertile branchlet nodes, gametangia geminate ................................................................................... C. braunii Bract cells few and short, gametangia always singular .......... C. evanida 3. Cortex absent from lowest internodes, gametangia geminate or clustered .................................................................................... C. karolii Cortex apparent on all mature internodes, gametangia singular............... ................................................................................................ C. muelleri

Type: not cited. Monoecious. Plants up to 110 mm high, rarely slightly annularly calcified. Axes 0.5–0.7 mm in diameter; ecorticate; spine cells absent. Stipulodes in a single whorl, 1 per branchlet, alternate, up to 1.5 mm long. Branchlets 8 or 9 in a whorl, up to 25 mm long, made up of 4–6 elongate ecorticated segments, terminated by a corona of 3 or 4 equal-sized cells, the basal branchlet cell up to 6 mm long. Bract cells 2, adaxial (occasionally 1 abaxial as well) at branchlet nodes, as long or longer than oogonia, 2 bracteoles shorter than the oogonium. Gametangia conjoined singly or in pairs at lowest 2 branchlet nodes. Oogonia up to 900 mm long, coronula up to 350 mm high, cells acute or apiculate. Oospores black 525–660 mm long, 310–410 mm wide. Striae of 9–10 wide (20 mm) ridges (pachygyra), basal-cell impression indented and 83–92 mm wide, wall smooth to smoothly fibrous. Antheridia up to 350 mm in diameter. Chromosomes reported by Wood (1971) for Australian material as n = 18; however, the specimen on which this count is based (Wood 61-3-24-5) was collected at the same time as a specimen of Nitella, and the specimen numbers could have been confused. Certainly n = 18 is more typical of Nitella than any species of Chara (Casanova 2015). Typification Specimens collected by Braun in the vicinity of Karlesruhe exist in several herbaria (e.g. GFW, MEL), and some of these may represent type material. The neotype selected by Wood and Imahori (1965) was collected from Italy, not Germany as indicated by Wood and Imahori. It comprises a small, somewhat immature specimen and may be superseded if original material can be subsequently located. Note The name C. braunii is retained for this taxon in Australia because of the overlap in characters with German material (C. braunii sens. str.) in the cluster analysis (Fig. 1). However, specimens in Australia differ from German C. braunii on the basis of coronula size and shape, and have consistently larger oospores (separation supported by the ordination; Fig. 2). As indicated in the introduction, a large number of infraspecific taxa have been described for this species. These taxa are not considered further in the present paper, pending detailed study of C. braunii sens. lat. elsewhere in its range. Etymology Named for Alexander Carl Heinrich Braun (1805–1877), botanist, charophytologist and director of the Berlin Botanic



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Fig. 3. Chara braunii from M.T.Casanova r422. A. Upper axis of mature plant; scale bar: 10 mm. B. Mature whorl of branchlets; scale: 5 mm. C. Gametangia conjoined singly, subtended by bracteoles, with no bract cells; scale bar: 200 mm. D. Branchlet apex with cluster of end cells (corona); scale: 200 mm. E. Geminate gametangia with bracteoles and one bract cell behind the oogonium; scale: 500 mm. F. Young, inflated branchlet whorl; scale bar: 1 mm. G. Scanning electron micrograph (SEM) of end-cell impression on the oospore; scale: 100 mm. H. Detail of oospore wall, showing development of ‘pachygyra’ striae and smoothly fibrous oospore wall; scale: 20 mm. I. SEM of oospore in side-view, with nine striae and smoothly fibrous oospore wall; scale: 100 mm.

Gardens (1851–1877). Braun collected the type material of C. braunii when he was 15 years old. Recognition Australian C. braunii is recognised on the basis of its ecorticate axis and branchlets and geminate gametangia.

Distribution Chara braunii is widely reported from Germany, Slovakia, Austria, Czech Republic, Denmark, Poland, Finland, Norway, Sweden, Russia, Greece, Albania and Iberian Peninsula (D˛a mbska 1964; Wood and Imahori 1965; Krause 1997), USA and Central America (Allen 1882) and the Middle East (Hussain

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and Khoja 1999). In Australia, C. braunii has been collected in the Gawler Ranges in South Australia and near Norseman in Western Australia. Von Mueller’s (1889) report of C. braunii from Pidinga (n.v.) is likely to be this species. Specimens examined WESTERN AUSTRALIA: Old Jimberlana Station near Norseman, 30 July 2000, B.Archer 1607 (MEL). SOUTH AUSTRALIA: Gawler Ranges National Park, Policemans Point offstream pool, 5 Oct. 2009, I.J.Powling s.n. (MEL); Gawler Ranges National Park, Policemans Point, 5 Oct. 2009, I.J.Powling s.n. (MEL); Gawler Ranges, Stove Drain, west branch, 5 Oct. 2009, I.J.Powling (M.T.Casanova r422) (MEL); Gawler Ranges, in a rock hole near the Dingo Fence and Lake Everard, 9 Aug. 2011, M.White s.n. (MEL).

Chara evanida Casanova, sp. nov. (Fig. 4) Type: VICTORIA: Lake Culluleraine, in ~300 mm of water within 10 m of the edge, close to the southern shore, 25 Nov. 2011, M.T.Casanova & S.A.Rosenbrock t903. Holo: MEL 2362669, iso: AD, B, BM, CANB, L, NY. Misapplications [Chara braunii C.C.Gmel. in Wood, R.D. 1971. Characeae of Australia. Nova Hedwigia 22, 22 spec. cit. 7.] [Chara braunii C.C.Gmel. in Casanova, M.T. and Porter, J.L. 2013. Two new species of Nitella (Characeae, Charophyceae) from arid-zone claypan wetlands in Australia. Muelleria 31, 53–59.]

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Fig. 4. Chara evanida from M.T.Casanova t903. A. Whole plant; scale: 50 mm. B. Whorl of branchlets; scale: 5 mm. C. Oogonium with mature, dehiscent antheridium; scale: 200 mm. D. End of branchlet with corona of cells; scale: 200 mm. E. Mature oogoinum and antheridium with bract cells and shorter bracteole, scale: 200 mm. F. SEM of oospore in side view with 9 striae and a smoothly fibrous oospore wall, scale: 100 mm. G. SEM of end cell impression at base of oospore, scale: 100 mm.



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[Chara braunii C.C.Gmel. in Porter, J.L. Kingsford, R.T. and Brock, M.A. 2007. Seed banks in arid wetlands with contrasting flooding, salinity and turbidity regimes. Plant Ecology 188, 215–234.]

(AD39117). VICTORIA: Winton Swamp, 14 Apr. 1959, H.I.Aston WS76 (MEL); Ovens River channel, 13 Jan. 2009, M.T.Casanova r228 (MEL).

[Chara braunii C.C.Gmel. in Casanova, M.T. 2009. ‘Seed bank analysis for the Condamine River, Macquarie Marshes and Ovens River catchments. Part I. Charophytes’. Unpublished report to Murray–Darling Basin Authority, Charophyte Services.]

Chara karolii Casanova, sp. nov.

Monoecious. Plants narrow, somewhat flexible, up to 160 mm high, without calcium carbonate deposition. Axes up to 400 mm in diameter, ecorticate throughout; spine cells absent. Branchlets 7–9 in a whorl, up to 23 mm long, segments 3–5, ecorticate, terminated by a corona of ~3 cells. Bract cells variable, in long plants in deep water they are hardly developed, in plants in shallow water they are as long or longer than the oogonia. Bracteoles 2, shorter than, to as long as, the oogonia. Stipulodes in one whorl, alternate, obscure or 0.2–1.5 mm long. Gametangia singularly conjoined at lowest 1 or 2 branchlet nodes. Oogonia 600–500 mm long (including coronula), 250–300 mm wide, 8 or 9 convolutions, coronula up to 150 mm high. Oospores black 360–670 mm long, 192–377 mm wide, 7–9 striae of thin flanges, basal-cell impression 80–130 mm in diameter, oospore wall smoothly fibrous. Antheridia up to 250 mm in diameter. Chromosomes not known. Recognition Chara evanida is recognised on the basis of its ecorticate axis and branchlets, and gametangia occurring singly rather than geminate or clustered. These features coincide with relatively small oospores (compared with other species in the group). There might be grounds in the future to separate plants with longer bract cells (occurring mostly in terminal wetland systems of the Murray–Darling Basin) from those in which the bract cells are obscure (generally found in riparian systems).

(Fig. 5) Chara aff. muelleri ‘Karol’, M.T.Casanova & I.J.Powling. Algae collected for the Lake Condah, Budj Bim Indigenous Protected Area Bush Blitz. Charophyte Services, Lake Bolac (2011).

Type: VICTORIA: Temporary wetland on ‘Lurnea’, Casanova Road, Westmere, 18 Nov. 2008, M.T.Casanova r167. Holo: MEL; iso: B, NY. Monoecious. Plants robust, up to 60 mm high, without calcium carbonate deposition. Axes up to 400 mm in diameter, 3-corticate in the upper internodes, ecorticate below; spine cells absent or rudimentary. Branchlets 8 or 9 in a whorl, up to 20 mm long, segments 3 or 4, ecorticate, terminated by a corona of ~3 cells. Bract cells 2 or 3 at branchlet nodes, bracteoles 2, as long as the oogonia. Gametangia conjoined, geminate or clustered at the lowest 2 branchlet nodes, as well as basal oogonia. Stipulodes in one whorl, alternate, up to 300 mm long, Oogonia 500–600 mm long (including coronula), 250–300 mm wide, 8 or 9 convolutions, coronula up to 150 mm high. Oospores black 480–660 mm long, 280–400 mm wide, 7 or 8 striae of low ridges, basal-cell impression 85–103 mm in diameter (25–30% of the diameter of the oospore), oospore wall with a reticulate pattern, when well developed the reticulum is constructed of small papillae on low ridges, the reticulae ~5 mm in diameter, the papillae ~0.5 mm in diameter on ridges ~0.5 mm high. Antheridia up to 200 mm in diameter. Chromosomes n = 14 (M.T.Casanova r933).

Distribution

Recognition

Chara evanida grows in eastern Australia, in wetlands and riparian systems in the Murray–Darling Basin, from southeastern Queensland to around Benalla in Victoria.

Chara karolii has corticated axes and regularly clustered gametangia (i.e. in twos and threes at each node), with the occasional occurrence of basal oogonia (the only instance of basal oogonia in this section), and granular or reticulately patterned oospores. Reticulate ornamentation on oospores in Chara is unusual. All other Chara species known possess either smooth, pustulate or porate, fibrous or granulate oospores (John et al. 1990, Leitch et al. 1990; Casanova 2005). Cortication is usually absent from the lowest axial internodes, and can be restricted to the very youngest internodes. Sometimes cortication is difficult to discern and a thorough check of the upper internodes is necessary. It is distinguished from species in section Agardhia with basal gametangia by its monoecy and corona of cells at the branchlet tips.

Etymology Evanida in Latin means ‘ephemeral’, in reference to the shortlived nature of the species, and its preference for temporary water bodies. Specimens examined QUEENSLAND: Warrill River, near Warwick, 11 July 1995, M.T.Casanova & M.A.Brock s.n. (NE65163); Waterloo Station, 8 July 2000, A.Emmott s.n. (MEL); Hutton Creek, C.R.Hornick Bridge, 3 July 2010, M.T.Casanova r709 (MEL). NEW SOUTH WALES: flooded rice field, Whitton, 20 Dec.1989, M.T.Casanova 891229-1c (NSW); flooded rice field, Whitton, 10 Dec. 1989, M.T.Casanova r984 (MEL); Gingham wetlands, 13 Mar. 2002, M.A.Brock 2GWZ (MEL); Gingham wetlands, 13 Mar. 2002, M.A.Brock 1GWZ (MEL); junction of the Murray and Darling Rivers, 1889, Mrs Holding s.n. (MEL); Macquarie Marshes, 11 Mar. 2002, M.A.Brock 20MMP (MEL); Macquarie Marshes, 11 Mar. 2002, M.A.Brock 1MMZ (MEL); Macquarie Marshes, 13 Jan. 2009, M.T.Casanova r227 (MEL); Momba Swamp, 31 Mar. 1999, J.L.Porter 209 (MEL); Tenterfield, 20 Nov. 1960, R.D.Wood 60-11-20-10A

Distribution Abundant in temporary wetlands in western Victoria, including the Budj Bim Indigenous Protected Area. There is a single specimen collected from the Northern Territory (R.Breen 25 Aug. 2014), which keys out to C. karolii (partly corticated axes and geminate gametangia) and is included here pending further study.

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Fig. 5. Chara karolii from A. M.T.Casanova r931 and B–J. M.T.Casanova r941. A. Whole plant, with somewhat contracted fertile whorls; scale: 10 cm. B. Whorl of branchlets; scale: 1 mm. C. Transverse section of axis showing cortical cells; scale: 500 mm. D. Gametangia arranged singly, with bract cells behind and beside, and bracteoles; scale: 500 mm. E. Branchlet tips with coronae; scale: 300 mm. F. Clustered gametangia; scale: 500 mm. G. Side view of oospore with eight striae; scale: 200 mm. H, I. Detail of oospore wall, showing incomplete and complete development of reticulate ornamentation; scale bars: 20 mm. J. End-cell impression on the oospore wall; scale: 100 mm. K. Chromosomes in two spermatogenous cells in metaphase, at 1000 magnification, n = 14.


Etymology Named for Kenneth G. Karol from The New York Botanical Garden, who first distinguished this species from C. muelleri on the basis of gene sequences (M.T.Casanova p474). Specimens examined VICTORIA: Byaduk, 12 Jan. 1962, A.C. 155 (MEL, NY); The Pinnacles, north of Mount Eccles, 17 Dec. 1960, A.C.Beauglehole 31 (MEL, NY); Anniversary Paddock Swamp, behind the dam, seed bank culture, 17 Nov. 2002, M.T.Casanova p474 (MEL, NY). Casanova’s Swamp below Lurnea Homestead, seedbank culture, 18 Nov. 2008, M.T.Casanova r167 (MEL); Chatsworth, dam in west paddock, Casanova’s property, 30 Nov. 2008, A.J.Casanova r197 (MEL); roadside ditch, Streatham–Eurumbeen road, 23 Nov. 2011, M.T.Casanova r931 (MEL); rubbish-tip swamp, Casanova Road, 28 Nov. 2011, M.T.Casanova r933 (MEL); Muldoon’s Sinkhole, Budj Bim Indigenous Protected Area, 28 Mar. 2011, M.T.Casanova r941 (MEL, NY); Tang Tang Swamp seedbank culture, 8 Jan. 2002, K.Ough Chara-b (MEL); Crabholes near Dimboola, s.d., F.M.Reader, s.n. (MEL). NORTHERN TERRITORY: creek above John Hayes Rockhole (Trepina), 25 Aug. 2014, R.Breen s.n. (MEL).

Chara muelleri (A.Braun) F.Muell. Trans. Roy. Soc. S. Australia 12, 149 (1889) (Fig. 6) Chara scoparia b muelleri A.Braun, Linnaea 25, 708 (1852); Chara scoparia b subsp.? muelleri (A.Braun) A.Braun in C.F.O. Nordstedt, Abh. Königl. Akad. Wiss. Berlin 1882, 118 (1883); Chara baueri f. muelleri R.D. Wood, nom. inval., Taxon 11, 14 (1962).

Type: In lacu Alexandrinae, 1848, F.von Müller, Holo: n.v.. Lecto: In aquis quid non procul a lacu Victoriae,A as ‘C. inconspicua’, MEL 2264893 (fide Wood 1971). Syn: nec non in stagnis ad lacum Victoriae, as ‘C. inconspicua’, MEL 2264892. Monoecious. Plants up to 15 cm high, without calcium carbonate deposition. Axes up to 640 mm in diameter; 2- or 3-corticate; spine cells absent or rudimentary. Branchlets 8 or 9 in a whorl, up to 2.8 cm long, segments 3 or 4, uncorticated, terminated by a corona of short cells. Bract cells 2 or 3 at branchlet nodes, 2 bracteoles 1–1.5 times as long as oogonia. Gametangia singularly conjoined at lowest 2 branchlet nodes. Stipulodes, in 1 whorl, alternate, up to 200 mm long. Oogonia 680–1400 mm long, coronula 250–340 mm high. Oospores black 680–1000 mm long, 480–600 mm wide. Striae of 7–9 ridges, fossa 90 mm across, wall smooth. Antheridia up to 300 mm in diameter. Chromosomes n = 28 (Casanova 2015). Recognition Chara muelleri has corticated axes and gametangia occurring singly. There are usually no spine cells on the axial cortication, and plants are often somewhat robust and inflated. Distribution Chara muelleri occurs in temporary water bodies, and at the temporary edges of permanent water bodies where there is little wave action, from the Fleurieu Peninsula in South Australia, in A


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eastern Victoria, northward to the Northern Tablelands of New South Wales. Etymology Named for the collector of the type material, Ferdinand von Mueller (1825–1896), director of the Royal Botanic Gardens Melbourne 1852–1888. Notes Wood’s (1962) combination Chara baueri f. muelleri is here treated as invalid, under Art. 41.5 of the ICN (Melbourne Code) (2012). Some specimens from Western Australia key out to Chara muelleri (e.g. Diels s.n., GFW; C.Tauss CT2885, MEL; M.N.Lyons 3249, PERTH); however, their oospores are much smaller and they are not included here pending further study. Specimens examined SOUTH AUSTRALIA: Cole Road Crossing seedbank culture, 7 Oct. 2004, M.T.Casanova p605 (MEL); Cherry Gardens, Mount Bold Reserve, 23 June 2000, E.Robertson 77 (AD108063). NEW SOUTH WALES: Dumaresq Dam, near boat ramp, 30 Oct. 1989, M.T.Casanova r980 (MEL); Racecourse Lagoon 1.6-m depth, 4 Sep. 1990, M.T. Casanova r981 (MEL, NE); dam off roadside, Wards Mistake Road, 2 Sep. 1990, M.T.Casanova r982 (MEL); dam opposite Black Mountain Roadhouse on Malpas Dam Road, 9 Aug. 1990, M.T.Casanova r983 (MEL); dam on the Malpas Dam Road, 11 Jan. 1994, M.T.Casanova p250 (MEL). VICTORIA: Snowy River, 1891, T.Cameron s.n. (MEL).

Discussion This is the first objective examination, based on a large number of specimens, of charophyte species with coronae on their branchlets in Australia. The approach has been conservative, with the description of two new species only, and confirmation of Chara braunii and C. muelleri for Australia. Proctor (1970) found that there were few reliable vegetative characters for separation of genetically isolated entities in the C. braunii complex, but concluded that specimens with regularly geminate gametangia were genetically isolated from those with solitary gametangia. Thus, in the present study, C. karolii (with clustered gametangia and oogonia at the base of the whorl) is separated from C. muelleri and C. evanida (both with solitary gametangia) and these are further separated from C. baueri and C. braunii, which have geminate and clustered gametangia. Proctor also found that for the majority of taxa within Chara, specimens from different continents were genetically isolated from one another. Despite this finding, material from Australia and the northern hemisphere is here referred to C. braunii on the basis of morphological similarity, and in the absence of a more thorough genetic analysis. Differences in the arrangement of gametangia are correlated with significant differences among the oospores of species in this group. Chara baueri has much smaller oospores (400–667 mm long, 183–300 mm wide) with very prominent ridges (pachygyra) than does C. muelleri (Pukacz et al. 2012). Chara karolii has a

Note: when Princess Alexandrina ascended the throne in 1837 she took the name Victoria. There was talk at the time of changing the name of Lake Alexandrina to Lake Victoria and this is likely to have been a source of confusion – e.g. von Mueller referred to the same lake (Alexandrina and Victoria) on the type material of this species.

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C A

B

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Fig. 6. Chara muelleri from A. M.T.Casanova p605, B–I. E.Robertson 77. A. Upper axis of narrow plant grown in culture; scale: 10 mm. B. Transverse section of axis with cortical cells; scale: 500 mm. C. Upper axis of somewhat inflated specimen; scale: 10 mm. D. Branchlet tip with corona; scale: 200 mm. E. Base of branchlet whorl with stipulodes and corticated axis; scale: 1 mm. F. Gametangia arranged singly, with somewhat inflated bract cells and shorter bracteoles; scale: 500 mm. G. Scanning electron micrograph (SEM) of oospore in side view with 10 striae; scale: 200 mm. H. Detail of oospore wall showing somewhat smooth surface; scale: 20 mm. I. Basal-cell impression on the oospore wall; scale: 100 mm.

granulate or reticulate ornamentation on the oospores, different from all others in this group, and C. evanida has much smaller, flanged oospores than does C. braunii from any location.

Several discrete groups can be detected within the Australian species described here, which correlate with smaller areas of distribution (groups identified as A–F in Fig. 1). The segregation


of these entities invites further investigation into their taxonomic status. Varietal and form status is not recognised here for Australian specimens, largely because the definition of those levels is controversial, and there is little support for such subdivision in recent genetic or phylogenetic studies (e.g. Sakayama et al. 2005). It is likely that morphologically discrete groups in separate areas will represent different breeding groups, quite possibly being genetically incompatible with each other through differences in chromosome numbers. Recognition of these as separate species could be possible in the future. The earliest gatherings of C. braunii and C. baueri in Europe were from water bodies in the vicinity of Karlesruhe and Berlin, respectively, and collections could still be made in the Berlin area until 1869 (Krause 1997). Examination of specimens collected by Bauer, Jahn and Braun in Australian herbaria indicated that there was some early confusion about these taxa (i.e. before ~1850) and some misidentifications were discovered in the present study (e.g. determination as C. braunii for corticated specimens). It is recommended that curators of European collections examine material collected in the early 1800s for correct determination. Although C. braunii has probably declined (still occurring in fresher waters associated with the Baltic Sea: Blindow 2000; within the Netherlands: Bruinsma 2010; the Czech Republic: Caisová and G˛a bka 2009), C. baueri disappeared and was thought to be extinct in Germany. Chara baueri has been recently recorded for the first time in temporary water bodies in Kazakhstan (Langangen and Sviridenko 1995) and rediscovered in temporary habitats in Poland and Germany (Pukacz et al. 2009, 2012). In contrast, C. muelleri, C. karolii and C. evanida are easily located if one searches in temporary ponds and wetlands in summer. All these species are summer-growing annuals, and they are probably all vulnerable to herbivory (Proctor 1999). In general, they grow rapidly and produce gametangia on the first whorl of branchlets (Casanova and Brock 1999a), and, consequently, the majority of specimens examined for the present study were fertile. They are rarely found in permanent waters, and have been seen to die out after a few months in outdoor culture (Casanova and Brock 1999b). Conservation of species in this group is entirely dependent on conservation of their habitat: temporary-, spring- and summer-filling shallow wetlands and riparian zones. These wetlands are often in agricultural settings (Pukacz et al. 2012) and vulnerable to changes in land management (Casanova 2012; Altenfelder et al. 2014). Although access to sites provided in the Bush Blitz program enabled the discovery of new charophyte species, and extended the ranges of others, one need not go to ‘wild places’ to discover new species of charophytes in Australia. Acknowledgements The Gunditjmara community, Winda Mara Aboriginal Corporation and the Lake Condah Sustainable Development Project are acknowledged for access to sites in the Budj Bim Indigenous Protected Area. For this study, access to type material in various American and European (B, BM, BP, GFW, GOET, HBG, L, LD, PC, NY and W) and Australian (AD, BRI, CANB, DNA, HO, MEL, NSW, PERTH) herbaria was essential. I thank the directors and staff of these institutions for their kind assistance and permission to remove oospores for examination. Many people have assisted with providing specimens, fresh


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and preserved, since 2000, some of their names are noted in the specimen lists. This study would have been impossible without their efforts. Beth Williams provided notes, translations and literature in an early part of this study. Mr Uwe Raabe is thanked for long-term discussion about the status of Chara muelleri and a field-trip to Poland and specimen of Chara baueri. Funds for this work were provided by the Australian Biological Resources Study grant number 209-49, Bush Blitz and Charophyte Services.

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