Keywords

Summary Classification

  • ●Charales

  • ●●Characeae Chara, Lamprothamnium, Lycnhothamnus, Nitella, Nitellopsis, Tolypella

Introduction

Charophytes are large, parenchymatous green algae (Fig. 1) that grow in fresh and occasionally in brackish water. Although less common than aquatic bryophytes or tracheophytes, charophytes are the ecologically dominant benthic macrophyte in some habitats. Charophytes are relatively large for green algae and can grow up to a half meter or more in height, in lush meadows and freshwater ponds, lakes, and flowing waters. The term “charophyte” used here applies to members of the order Charales , which contains extant and fossil taxa (Feist et al. 2005).

Fig. 1
figure 1

Charophyte thallus morphology. (a) Chara drummondii; (b) Nitella haagenii; (c) Lampro-thamnium macropogon; (d) Tolypella polygyra. (M. T. Casanova)

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Charophytes have a complex thallus with an upright, stemlike main axis punctuated by whorls of branchlets (Fig. 1). Rhizoids anchor the thallus in sandy or muddy substrates. Thalli of some genera (notably Chara, Lamprothamnium, and Tolypella) accumulate calcium carbonate externally and have a musky odor. Worldwide in distribution and occasionally abundant in submerged areas, these macroscopic green algae have been well studied for several centuries by biologists (e.g., Allen 1888, 1889; Braun and Nordstedt 1882; Corillion 1972) .

Six extant genera in the family Characeae and order Charales are recognized; two additional orders and a large number of genera and families are known from the fossil record (Table 1). Two extant genera are common: Chara and Nitella, each with several hundred species. Of the other four genera, Tolypella and Lamprothamnium are the most common and diverse, with approximately 16 and 7 species, respectively. A monograph by Wood and Imahori (1965) synonymized numerous species in Chara and Nitella and recognized only 19 species in Chara and 50 in Nitella, with numerous subspecific taxa. Wood’s taxonomic arrangement has not been widely adopted due to experimental work showing that the earlier taxonomy reflected species-level differences in terms of reproductive isolation (e.g., Grant and Proctor 1972; Proctor 1975; McCracken et al. 1966). Therefore, earlier species names are commonly used in the current literature.

Table 1 Classification of green algae commonly known as charophytes (Modified from Feist et al. (2005) and Lewis and McCourt (2004))
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The charophyte thallus is composed of basal rhizoids, with an upright axis consisting of alternating internodes and nodes. Due to their large size and apparent complexity, charophytes may be mistaken for bryophytes or certain aquatic angiosperms (e.g., Ceratophyllum) in the field. Charophytes lack the diploid sporophyte generation and multicellular embryos of bryophytes and vascular plants (Graham and Wilcox 2000). However, their plantlike structure, complex asymmetric sperm, and large, protected egg cells (described below) led earlier workers to see them as intermediate in complexity between green algae and embryophytes (Bold and Wynne 1978; Smith 1950). This intermediate position was clarified by molecular studies that show charophytes to be one of several groups of green algae that are more closely related to land plants than they are to the rest of the green algae (Karol et al. 2001; Lewis and McCourt 2004; McCourt et al. 2004; Turmel et al. 2006).

Charophytes fulfill a number of ecological roles in both permanent and temporary water bodies (van den Berg et al. 1998). They are primary producers, sometimes the dominant photosynthesizers in aquatic ecosystems (Schwarz et al. 1999; Porter 2007). Stands of charophytes provide habitat for epiphytic algae, invertebrates (Hawes and Schwarz 1996; James et al. 1998), and structural refuges for zooplankton (Kuczyńska-Kippen 2007) and juvenile vertebrates (fish and frogs). Charophytes are often early colonizers and water clarifiers (Casanova et al. 2002), and they are directly consumed by a number of arthropods (beetles, amphipods; Proctor 1999) and snails (Elger et al. 2004), fish (Lake et al. 2002), and water birds (Schmieder et al. 2006). In deep lakes they can be the deepest growing plants (Dale 1986; Schwarz et al. 1999). Charophyte communities in temporary wetlands are commonly species rich (Casanova and Brock 1999a) occurring as individual plants (Casanova and Brock 1999b), although monospecific, continuous “beds” or “meadows” are also common (Stross et al. 1988; Pelechaty et al. 2010).

Charophyte life histories are haplobiontic, with one free-living haploid vegetative phase. After meiosis in the zygote, the haploid oospores germinate and produce a protonema, which differentiates into axes, branchlets, and rhizoids at the first node. The rhizoids grow downward (Kiss and Staehelin 1993), anchoring the thallus axis in the sediment, and the axes grow upward (Andrews et al. 1984). Sexual reproduction may be initiated either as soon as possible after germination (e.g., Chara muelleri, Casanova and Brock 1999a) or in response to environmental cues (e.g., Chara australis, Casanova 1994). Life histories can be annual or perennial (Casanova and Brock 1999a), with annual species most frequently occurring in habitats subject to periodic drying (Blindow 1992a, b) or freezing (Schwarz et al. 1999). However, some species (e.g., Chara braunii) with an annual life history occur in areas exposed to long-term flooding (Casanova and Brock 1999b).

Practical applications for charophytes include management of water quality (through encouragement of charophyte colonization) and as an indicator of water regime requirements in riparian and wetland ecosystems (Casanova 2011). Because their large cells are easy to observe and manipulate, charophytes have been useful as model organisms for studies of cell membrane potential and cytoplasmic streaming (Tazawa et al. 1987; Tazawa and Shimmen 2001; Raven and Brownlee 2001; Yamamoto et al. 2006).

Habitats and Ecology

Charophytes are primarily freshwater plants, but they are occasionally abundant in brackish areas, both in contemporary habitats (Shepherd et al. 1999) and in ancient ones, as shown in the fossil record (Soulié-Märsche 1999; 2008). These algae usually occur in quiet or gently flowing waters, from very shallow (several cm) to deep (>10 m (30 m in clear lakes such as Tahoe)), so long as light and oxygen levels are adequate. Some have been found in swiftly flowing rivers (personal obs.), but such occurrences have been rarely noted in the literature. Habitats are typically alkaline (hard water), although some species are known from mildly acidic waters. Rhizoids are usually anchored in sandy substrates mixed with gravel. The upright portions of plants are buoyant and exhibit a characteristic whorled pattern when viewed from above (Casanova 2009).

The family Characeae, which contains all living charophytes, is worldwide in distribution, but individual species range from restricted endemics to broadly distributed taxa. In general, dioecious taxa are narrowly distributed or endemic, whereas monoecious taxa are usually widely distributed (Proctor 1980).

Autecological studies predominated in the early literature, in which species distributions were characterized by environmental parameters (e.g., temperature, light, depth, water quality characteristics) (Hutchinson 1975). Interspecific interactions have not been investigated as thoroughly, but competitive effects of vascular plants and algae on charophytes have been suggested (Stross 1979; Stross et al. 1988). In fact, Martín-Closas (2003) hypothesized that charophytes dominated freshwater floras after the Permian until angiosperms evolved and came to dominate freshwater habitats from the Lower Cretaceous until the present.

Nutrients are absorbed by charophytes through their rhizoids and photosynthetic thallus (Kufel and Kufel 2002), and charophyte communities can be a significant store of nitrogen in small water bodies (Rodrigo and Alonso-Guillén 2008). Uptake by charophytes removes nutrients from the water column that would otherwise be available for growth of other algae (van den Berg et al. 1998; Siong et al. 2006). In addition, some species have an allelopathic effect on the growth of certain microalgae (Blindow and Hootsmans 1991; Pakdel et al. 2013). Early reports by Forsberg (1964) that even low concentrations of phosphorus were toxic to charophytes have not been supported by subsequent studies (Blindow 1988) and the decline of charophytes following eutrophication can be explained largely by decreases in water clarity and competition with angiosperms (Blindow 1992a).

Susceptibility or resistance to predation has been shown to determine the presence or absence of charophytes in various permanent and ephemeral habitats (Mann et al. 1999; Proctor 1999). A number of studies have investigated the marked zonation of charophytes in lakes, a pattern where charophytes grow in a discrete band with distinct upper and lower depth limits. Studies have invoked light, competition, and herbivory as the controlling factors that set the depth limits (Schwarz et al. 1999, 2000).

Charophytes are well adapted to the submerged aquatic environment. For example, the evolutionary significance of the multinucleate giant cells of charophytes has been explained as a shade-tolerance adaptation (Raven et al. 1979) by which cytoplasmic streaming in giant cells of charophytes optimizes transport of nutrients to various parts of the thallus, analogous to the phloem-like system of transport that evolved in kelps or other large algae.

Characterization and Recognition

The charophyte axis has a distinctive node-internode structure. Internodes consist of so-called giant cells, which are multinucleate. Nodes comprise several, smaller, uninucleate cells that give rise to whorls of leaflike organs of limited growth called “branchlets,” and secondary axes (branches of unlimited growth), which also exhibit the node-internode construction. A single apical meristematic cell occurs on each axis tip, the latter exhibiting a pattern of growth and branching similar to the apical meristem of higher plants (Fig. 2) (Cook et al. 1998; Pickett-Heaps 1975; Clabeaux and Bisson 2009). Internodes are composed of giant cells, which are multinucleate with numerous ellipsoidal plastids distributed in the cytoplasm surrounding a large central vacuole. The cytoplasm streams actively lengthwise around the cell periphery. Internodal cells may be naked or covered by a single-celled layer of thin cortical cells that grow upward and downward from nodal cells to cover the internodes. Some corticating cells project outwardly as spines. Cortication is common among species of Chara, incomplete in the rare genus Lychnothamnus, and absent in Lamprothamnium, Nitella, Nitellopsis, and Tolypella. Shape and numbers of ranks of cortical cells are important in delineating species in Chara (Wood and Imahori 1965; Casanova 2005).

Fig. 2
figure 2

Apical meristem of Chara, longitudinal section. Large intermodal cells show a clear, central vacuolar region; lateral branchlets arise from peripheral cells at nodes. (Photograph courtesy of Dr. Martha Cook, from a specimen from Ward’s Natural Science)

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Nodes consist of several uninucleate cells produced through cytokinesis of 1–3 central cells that give rise to a series of peripheral cells (Cook et al. 1998), with adjacent cells connected by true plasmodesmata. These peripheral cells are initials that give rise to branchlets 3–10 cells in length or to secondary axes that exhibit the node-internode structure of the main axis. Peripheral cells are also the initials for the cortical cells and for stipulodes. Stipulodes are single cells that subtend branchlet whorls at nodes. They may be short and blunt or long and tapering, and they occur in one or two tiers. Stipulodes are present in Chara, Lamprothamnium, and Lychnothamnus in the tribe Chareae and absent in Nitellopsis and the Nitelleae (see “Classification” section below).

Growth occurs through division of an apical cell at the tips of the main axes or secondary branches. A single cutting face of the apical cell produces an alternation of internodal cells and nodal initials. The nodal initials develop into the nodes through the cytokinetic pattern described above. While the apical region in charophytes (Fig. 2) is superficially similar to the apical meristems of higher plants (Pickett-Heaps 1975; Clabeaux and Bisson 2009), the single cutting face is simpler than meristematic development in higher plants (Cook et al. 1998). Cook et al. (1998) interpreted the presence of plasmodesmata and pattern of cytokinesis as a parenchymatous organization of nodal tissue. In this interpretation the internodes and cortical cells are filamentous in construction, whereas the nodes are parenchymatous plates, similar to the earliest histogenetic tissues of plant apical meristems. Homology of these tissues in Charales and higher plants is open to question.

Branchlet morphology differs greatly among genera (Fig. 1). Chara, Lamprothamnium, and Lychnothamnus produce whorls of branchlets that are essentially monopodial and do not branch dichotomously. Branchlets in Nitella are generally not monopodial, and they bifurcate one or several times at the nodes. Tolypella, the third common genus, exhibits clusters of branchlets and stalked reproductive structures in clusters at nodes that have the appearance of a bird’s nest.

Asexual reproduction occurs through growth of erect axes from nodes on the rhizoids, and through contracted starch-filled branches (Casanova et al. 2007; Casanova 2009), and tubercular, starch-filled outgrowths of the rhizoids called bulbils (Fritsch 1948; Casanova 1994), which may fall away and germinate separate from the thallus.

Sexual reproduction is oogamous. Oogonia and antheridia are the female and male gametangia, respectively, which include gamete-producing cells and associated vegetative cells. Each oogonium contains a single large egg cell, whereas sperm are produced in filaments with numerous antheridial cells, packed inside a spherical antheridium (Pickett-Heaps 1975; Graham and Wilcox 2000). Smith (1950) interpreted the oogonia and antheridia as single-celled structures, each within a larger structure of modified sterile vegetative filaments. He and some authors used the terms “globule ” for the male and “nucule ” for the female sexual structures, although the more common terms used are antheridia and oogonia, or oosporangia, respectively. Oogonia and antheridia occur on the branchlets at nodes and may be associated with small sterile cells and can be enveloped in mucous. The oogonia are oblong, 200–1000 μm long by 200–600 μm wide. Sexual structures are easily visible with a hand lens or even with the naked eye. Thalli may be dioecious or monoecious. In monoecious species, the two kinds of reproductive structure may occur at the same node (conjoined) or different nodes (sejoined) on the same branch. Sexual structures are relatively easy to remove for experimental crossing studies of monoecious and dioecious species (McCracken et al. 1966; Grant and Proctor 1972).

The egg is surrounded by five jacket cells that spiral in a left-handed (sinistral) twist from the base to the apex, which consists of one or two tiers of cells that form a corona (Fig. 3). The Chareae have one tier of coronal cells, the Nitelleae two. The mature oospore (Fig. 4) displays a basal pentagonal cell and in some genera one or two additional basal cells.

Fig. 3
figure 3

Apex of Chara oogonium (female sexual structure) with single tier of five coronal cells. Note spiral jacket cells and transparent sperm swimming around apex. (M. E. Cook)

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Fig. 4
figure 4

SEM images of oospores of Characeae showing single-celled (a) and two-celled (b) basal plate. (a) Chara muelleri. (b) Nitella sp. Specimens of both collected from western Victorian swamps, Australia. (M. T. Casanova)

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Male antheridia are spherical and range from 200 to 1500 μm in diameter, often bright orange in color. The outside of the antheridium is composed of four or eight shield cells, inside of which is a cluster of modified multicellular filaments, each cell of which produces one sperm. Sperms have two flagella attached slightly below the apex of an asymmetric, helically twisted cell reminiscent of sperm cells in mosses and liverworts (Renzaglia and Garbary 2001).

Sperm cells are liberated when the shield cells separate. Sperm gain access to the egg cells through slits between jacket cells near the apex of the globules (Fig. 3). The zygote and inner jacket cell walls thicken, and the outer parts of the jacket cells fall away leaving an oblong, spiral-embossed spore, which may germinate immediately or go through a period of dormancy (Casanova and Brock 1996). Upon germination, a main axis and a rhizoidal initial are produced, which develop into the mature thallus (Fritsch 1948).

The Characeae possess large chromosomes (Fig. 5) that are relatively easy to stain and count during mitotic cell divisions (Casanova 1997). Young antheridia provide the best material for chromosome observation, but rhizoid squashes can also be successful. Chromosome numbers vary widely in all genera. Counts between 8 and 77 have been published as observed values within Chara and Nitella (Guerlesquin 1984; Bhatnager 1983). On the basis of this multiplicity of published numbers, both Bhatnager (1983) and Guerlesquin (1984) have attempted to identify the basic or ancestral chromosome numbers for the group. Not surprisingly, the plethora of reported chromosome counts has resulted in basic chromosome number(s) for Characeae of 3, 5, 6, 7, 8, or 11. Grant (1990) hypothesized that a single base, or ancestral, number of n = 14 is adequate to explain all extant chromosome numbers in the genus Chara and that aneuploidy is either extremely rare or absent. He noted that reported chromosome numbers in Chara were invariably multiples of 14, i.e., 14, 28, 42, or 56, in natural populations. Estimates of chromosome numbers in Nitella range from 3 to 27, almost invariably multiples of 3 or 9, so the basic chromosome number is likely to be 3. Grant (1990) also argued that the cytogenetic mechanism and evolutionary history of this group cannot be well understood until chromosome numbers are established and that chromosome counts must be stable and correlated with biological species and not the result of an aberrant cell division product. Further karyotypic work on the Characeae is clearly needed. Grant and Proctor (1972, 1980) postulated that polyploidy is adaptive as a mechanism for producing (and masking harmful) genetic variation in self-fertilizing monoecious species, in contrast to dioecious species, which generally possess half the number of chromosomes. In dioecious species, genetic variation maintained through outbreeding may enhance survival in habitats that vary from one generation to the next (e.g., in temporary wetlands), and in polyploid monoecious species, variation in enzyme activity (through multiple copies of enzymes) is likely to enhance survival during the life of a single plant or population (e.g., in permanent habitats) (Casanova 1997). Grant and Proctor (1972, 1980) suggested that sexual reproduction functions as a mechanism of dispersal and drought avoidance in addition to its role in genetic recombination.

Fig. 5
figure 5

Metaphase mitotic chromosomes of Chara, Nitella, and Lamprothamnium. (Photograph courtesy of Michelle Casanova). (a) Nitella leonhardii, n  =  28. (b) Lamprothamnium inflatum, n  =  14. (c) Chara globularis, n  =  42. (M. T. Casanova)

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Classification

The genus Chara was erected by Vaillant in 1719 for several living species of this genus and formally recognized by Linnaeus (1753) as one of several genera of algae. Understanding of the relationship of the Charales to other green algae and land plants has undergone considerable revision in recent years (reviewed in McCourt et al. 2004; Becker and Marin 2009). The relatively complex morphology and reproduction of charophytes has been long known and led Smith (1950) and others (Margulis et al. 1990, in the first edition of this book) to view the group as a class (Charophyceae) separate from the rest of the green algae (Chlorophyceae). Some workers preferred to elevate the group to division status (e.g., Charophyta of Bold and Wynne 1978). Research on cell ultrastructure and flagellar insertion (Mattox and Stewart 1984), along with molecular phylogenetic studies (McCourt et al. 1996, 1999; Meiers et al. 1999; Karol et al. 2001; Sakayama et al. 2002; 2004a, b, 2005a, b), supported the monophyly of extant members of the group, regardless of rank. In addition, the monophyly of the fossil and extant members of the Charophyceae is well supported (Feist et al. 2005). Figure 6 depicts a consensus molecular phylogeny for the genera of extant Charales (Karol et al. 2001) and also shows the occurrence record of fossils for the major lineages since the origin of the group in the Silurian (dates from Feist et al. 2005). Note that some sister lineages of the extant Charales occur much earlier in the fossil record (Early Devonian) but have since become extinct.

Fig. 6
figure 6

Phylogenetic relationships of genera in the Charales, and ranges of fossil ages of extant genera and several extinct taxa. The black bars indicate the ages of the earliest known fossils for taxa, as well as fossil ages for extinct taxa in the Charales and the extinct Orders Sycidiales and Moellerinales. Relationships of extant taxa based on molecular phylogenetic studies (McCourt et al. 1999; Meiers et al. 1999; Karol et al. 2001). Fossil ages and phylogenetic relationships of fossil taxa based on Feist et al. (2005). (R. M. McCourt and J. D. Hall)

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Feist et al. (2005) summarized the history of classification of the charophytes and proposed a classification including both fossil and extant taxa in the phylum (=division) Charophyta, with the single class Charophyceae. Living charophytes are included in the family Characeae in the order Charales, along with five families of extinct taxa known primarily from fossil spores (gyrogonites), with few vegetative thalli in the fossil record (but see Kelman et al. 2004). Two additional orders of fossil taxa (Fig. 6) are also included in the Charophyceae (Feist et al. 2005).

Lewis and McCourt (2004) proposed a classification of green algae that assigned extant charophytes to the class Charophyceae in a clade containing several other orders of green algae plus embryophytes or land plants. A separate clade comprises the remaining members of the traditional Chlorophyta. This division of the green algae into two evolutionary lineages, one of which contains several smaller groups (Chlorokybophyceae, Klebsormidiophyceae, Coleochaetophyceae, by Cook and Graham) and the other larger clade of conjugating green algae (Zygnematophyta, by Hall and McCourt), was originally based on ultrastructural morphology of flagellar roots and types of mitosis, as well as features of glycolate metabolism (Mattox and Stewart 1984). The hypothesis of two major clades has been strongly supported by molecular data (McCourt et al. 1996; Karol et al. 2001; Becker and Marin 2009). In this scheme, the green algae sensu lato do not constitute natural group, and some green algae are clearly more closely related to embryophytes than to other green algae (i.e., Charophyta sensu Karol et al. 2001). A classification of charophytes of this chapter is shown in Table 1.

The evolutionary relationship of Charales to embryophytes remains unresolved (Graham 1993; Lewis and McCourt 2004; Turmel et al. 2006; Becker and Marin 2009). Karol et al. (2001) performed a phylogenetic analysis on a broad sample of 35 green algae and embryophytes using four genes (two plastid, one mitochondrial, one nuclear, ~5000 bp) and found strong support for the hypothesis that the Charales are the sister group (i.e., closest living relatives) of land plants. This hypothesis has been challenged by a study of entire plastid genomes from a smaller number of green algae and land plants (Turmel et al. 2006). The latter study used 76 genes from the complete plastid genomes of nine green algae and embryophytes (~48,000 nt) and found strong support for the hypothesis that conjugating green algae (see Zygnematophyta) constitute the sister group to embryophytes. These alternate hypotheses of the embryophyte sister taxon would lead to very different sets of assumptions about the common ancestor of embryophytes and their nearest green algal relative, since the Zygnematophytes are simpler in morphology and reproduction than the charophytes and lack mastigote cells entirely (McCourt et al. 2004). Some of the implications of the sister status of Zygnematophytes and embryophytes are explored in Wodniok et al. (2011).

Additional data with more taxa and more sequence data (including organellar genome data) may resolve this interesting question with significant implications for the evolution of land plants and the origins of their adaptations to a dry habitat.

Maintenance and Cultivation

Charophytes present some unique challenges for cultivation due to their size, life cycle, and, in some cases, dioecy. The erect thallus and rhizoid system often require larger culture vessels (liter sized or more) for the development of adult morphology. The effort needed for culturing charophytes depends on the uses to which they will be put and the length of time the cultures will need to be maintained. Short-term cultures for physiological studies (Beilby and Shepherd 2006), chromosome assessments (Casanova 1997), teaching exercises, or morphological studies (Casanova 2009) can be simply obtained from field-collected material kept in rainwater on a windowsill. Longer term cultures for genetic vouchers or clonal reproductive studies are more difficult to maintain. Because epiphytes are frequent, axenic cultures are difficult to establish from vegetative material. Unialgal cultures (i.e., with a single species of eukaryotic algae and possible bacterial contamination) can be obtained through germination of surface sterilized spores in defined media. However, material for microscopic observation and molecular studies can usually be obtained from branch tips that are relatively free of epiphytes.

Proctor (personal communication) developed a successful means of growing what he termed “clones” (isolates from single vegetative thalli or oospores) in seminatural conditions in a greenhouse. In this method, wide-mouth one-gallon (3.8 L) glass jars are filled to a depth of 3 cm with autoclaved or steam-sterilized alkaline sandy-loam soil. Jars with sandy loam are filled with steamed or filter sterilized water free of chlorine and metal residue from copper pipes. Field-collected sprigs of vegetative branches brushed or manually cleaned of epiphytes are then planted in the sandy loam using clean large forceps or gloved hands. After several weeks, it will be apparent if the sprig has successfully anchored itself in the sediment with rhizoids. Epiphytes or algal cells associated with the field-collected sprigs may infest some cultures, but the Proctor reported (personal communication) that these often die back without any special treatment. While not always successful, this technique can yield long-lived (>20 years) clonal cultures that require little more than indirect sunlight on a window sill. Such cultures are readily used in the classroom.

The National Institute for Environmental Studies in Japan (NIES; http://mcc.nies.go.jp/) has reported success in growing charophytes in defined media and provided illustrated instructions on culture methods. Watanabe (2005) has also provided methods for ex situ cultivation of threatened algal species and included media for Charales.

Evolutionary History

The Charales are exceptional among green algae in having an extensive fossil record, rivaled only by the Dasycladales of the Ulvophyceae (Berger and Kaever 1992; Taylor et al. 2009). Some taxa of both groups deposit calcium carbonate as part of the thallus, which facilitated formation of fossils of vegetative and, in particular, reproductive structures (spores). In Charales, the oogonium is often enveloped by a calcium carbonate “shell” (most Nitella and some Chara species are exceptions). Fossils resulting from these types of reproductive structures are called gyrogonites, which are often more elaborate in structure than spores of extant Characeae (Fig. 7). Gyrogonites range in size from a few hundred μm to several mm in size. Although some vegetative thalli may be calcified, such as the well-known Paleonitella found in the Early Devonian Rhynie chert (Kidston and Lang 1921), gyrogonites are much more common in the fossil record. Therefore, gyrogonite morphology is the basis for most of the taxonomy and stratigraphy of fossil Charales (Feist et al. 2005).

Fig. 7
figure 7

Gyrogonite of Maedleriella angusta Feist-Castel, a species from the Middle Eocene of Southern France (From Feist-Castel 1972)

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Morphology of gyrogonites provides a rich source of data: shape, dimensions, apical structure, presence and absence of pores, morphology of membranous coverings that occur in some groups, occurrence of a variety of bumps, tubercles, or other ornamentations on the outer surface (Feist et al. 2005). The earliest gyrogonites from the late Silurian and Early Devonian exhibit greater morphological variation than oospores or more recent or extant taxa. The pattern of spiraling of the jacket cells (also called spiral cells) apparently reversed in the Early Devonian (ca. 370 mya) from dextral to sinistral, and the number of jacket cells decreased over time such that all extant taxa now have five sinistral jacket cells, although occasionally spores with six cells are found (M. Casanova, personal observation).

Between the upper Silurian and the present day, charophytes have gone through several periods of diversification and extinction (Grambast 1974). Diversity was greatest during the Devonian, with a secondary peak in diversity in the Late Jurassic and Early Cretaceous (Feist et al. 2005). Since the Miocene, diversity has declined (Grambast 1974) so that only a single family (Characeae) with six genera survives today. Feist et al. (2005) provided a comprehensive overview of the fossil record and evolutionary history of the group.