Biology and functional ecology of Equisetum with emphasis on the giant horsetails.
Equisetum is the only remaining representative of the once abundant and diverse subdivision Sphenophytina. The 15 living species of the genus comprise the plants commonly known as horsetails. The antiquity an uniqueness of the genus has inspired sustained interest in the botanical community and a rich literature (Reed, 1971). The genus name is derived from the Latin equis, meaning horse and seta, meaning bristle, in reference to the coarse black roots of Equisetum fluviatile which resemble a horse's tail (Hauke, 1993). The horsetails range in size from the diminutive E. scripoides (stems averaging 12.9 cm tall and 0.5-1.0 mm diameter) (Hauke, 1963) to the giant horsetails, E. giganteum and E. myriochaetum, reaching heights of 8 or more meters (Hauke, 1963) and stem diameters of ca. 4 cm. Equisetum species are vascular plants which reproduce sexually by means of spores that are borne on cones. Hence, together with the other spore-bearing vascular plants, the Lycophytes (club mosses), Psilophytes (whisk ferns) and Pterophytes (true ferns), Equisetum species are classified as pteridophytes. However, recent molecular phylogenetic studies suggest that Equisetum should be classified within the monilophytes (Karol et al., 2010; Pryer et al., 2001; Qiu et al., 2007). In fact, Equisetum, ferns and Psilophytes appear to be closer to seed plants (to which they form a sister group) than they are to Lycophytes, making the traditional classification of "pteridophyte" one of convenience only (Kranz and Huss, 1996; Qiu et al., 2007). The placement of Equisetum within the monilophytes remains unclear, with certain markers providing weak support linking the genus with the Marattiaceae (Pryer et al., 2001; Qiu et al., 2007) and a large number of plastome genes providing moderate support for a sister relationship with Psilotum (Karol et al., 2010). Like both of these families, horsetails are eusporangiate. Interestingly, affinity between the gametophytes of Equisetum and those of eusporangiate ferns was recognized as early as the 1920's (Campbell, 1927).
However, enigmas remain in the placement of Equisetum within vascular plants, because inclusion of fossil taxa in the phylogeny creates a different picture, but with Equisetum still allied more closely to ferns than with Lycophytes (Rothwell and Nixon, 2006). Furthermore, Equisetum cell walls have recently been shown to contain a hemicellulose, (1 [right arrow] 3,1 [right arrow] 4)-[beta]-D-glucan, thought to be unique to the Poales that is not shared by eusporangiate ferns (Equisetum's closest relatives according to molecular data), Psilotum, or Lycophytes (Fry et al., 2008b; Sorensen et al., 2008; Knox, 2008). This hemicellulose may be linked to silica accumulation and deposition (Fry et al., 2008b). In addition, Equisetum contains a cell wall remodeling enzyme that it appears to share only with Charophytic algae, not with other pteridophytes (even the the most basal pteridophytes, the Lycophyes) (Fry et al., 2008a). Further evidence of the uniqueness of the genus is provided by two introns that the genus shares with the liverwort Marchantia, but that are not round in other vascular plants, including lycophytes (Begu & Araya, 2009). Bower (1908) noted that the early embryonic assertion of the stem axis in Equisetum and only significantly later and secondary formation of the first leaf sheath, would be expected in ancestral vascular plants. In contrast, cotyledons assert early in the embryo development of Lycopodium (Bower, 1908). These observations are intriguing evidence of the extreme isolation of the genus Equisetum and its retention of ancient features. Remarkably, the modern genus Equisetum has a history stretching back to the Jurassic (Channing et al., 2011) and possibly as far back as the Triassic (Hauke, 1978). As a result, Equisetum may perhaps be the oldest living genus of vascular plants (Hauke, 1963).
All Equisetum species are herbaceous perennials. The plant consists of upright aerial stems that arise from a very extensive underground rhizome system (Hauke, 1963). Morphologically, the genus Equisetum is characterized by jointed aerial stems and jointed rhizomes. The stems of horsetails are "anatomically [...] unique among plants" (Niklas, 1997) (Fig. 1a) although they have an external appearance somewhat reminiscent of bamboo. The upright aerial stems exhibit a monopodial branching pattern, having one main axis of growth. This is the pattern which is also round in most gymnosperms and angiosperms (Scagel et al., 1984). Equisetum species also have small microphyllous leaves that are arranged in true whorls (Rutishauser, 1999) and the leaves of each whorl are fused together to form a cylindrical sheath around each node (Hauke, 1993) (Fig. 1d). Some, but hOt all, species form whorls of lateral branches at the nodes of the aerial stems (Hauke, 1993). The aerial stems, but not the rhizomes, of some species die back seasonally, whereas other species are evergreen. Rhizomes have the same general morphology as upright stems (Fig. 1b), although rhizomes bear adventitious roots (i.e. roots arising from the stem rather than from other roots) at their joints in addition to leaf sheaths and branches (Fig. 1c). Aerial stems range in height from the 8 m high tropical species, E. myriochaetum, to the 4-5 cm tall temperate species, E. scirpoides (Hauke, 1963).
Stem lengthening is produced by intercalary meristems above each node and this growth pattern produces a relatively rapid extension (Stewart & Rothwell, 1993). This is a process similar to that which occurs in bamboo, which also have stems that lengthen primarily via intercalary meristem growth (Judziewicz et al., 1999). The nature of stem elongation in Equisetum is easy to observe. In developing stems, the region of the internode close above a node is noticeably lighter green than the internode further away from the node. This is because the internode tissue nearer the node is more recently generated by the intercalary meristem and is therefore less mature than tissue farther away. Two types of elongation meristems are found in Equisetum rhizomes. French (1984) found that the three subgenus Equisetum species he studied had uninterrupted meristems "charactersized by acropetal internode maturation". In contrast, the four species of subgenus Hippochaete that he studied had intercalary meristems in their rhizomes.
Beyond typical Equisetum morphology, several interesting aberrations have been observerd (Schaffner, 1933). These include a spiraling entire leaf sheath along the length of the stem, as opposed to the normal separation of each sheath and lack of any spiraling (Schaffner, 1927, 1933; Tschudy, 1939; Bierhorst, 1971). Other peculiar teratologies include flexuous stems, extremely short internodes, dichotomous branching of shoots, cones that continue vegetative growth, and cones borne on the lateral branches of species that normally only have a cone at the apex of the central stem (Page, 1968; Schaffner 1924, 1933; Tschudy, 1939; Westwood, 1989). In general, the appearance of Equisetum shoots can be remarkably plastic in response to the environment (Hauke, 1963; Schaffner, 1928). These abnormalities and plasticities may provide clues to understanding the development of the unique architecture and ecology of Equisetum. They may also provide clues as to the origins and ontogeny of vegetative and reproductive structures within extinct Sphenophyta.
Unique Characteristics of the Genus Equisetum Among Vascular Plants
Lateral Branch Origin
Unlike all other vascular plants which produce branches exogenously (and most in the axils of leaves), the branches of Equisetum are produced endogenously (Hofmeister, 1851; Stutzel & Jadicke, 2000) and, furthermore, the leaves of Equisetum alternate with branches at each node (Scagel et al., 1984) (Fig. 1d). In other plants with lateral (as distinguished from terminal) branching, branches originate in leaf axils (i.e. in the vertex of the upper angle between a leaf and the stem from which it arises)
Dayanandan (1977) observed that Equisetum species "possess perhaps the most structurally complex stomata in the entire plant kingdom" (p. 175). The stomata of equisetum are so unique that "a single well-preserved stomatal apparatus is all that is needed to identify the genus Equisetum (even the two subgenera) from among all other living plants" (Dayanandan, 1977). The uniqueness of Equisetum stomata is the result of two characteristics (Dayanandan, 1977):
1.) The two subsidiary cells overlie the guard cells completely, whereas in other plants the guard cells are the superficial cells.
2.) "The inner tangential wall of each subsidiary cell develops 7 to 24 ridge-like thickenings, a feature not found in any other genus." (Dayanandan, 1977)
Each Equisetum spore has four strap-like structures called elaters attached to the spore surface at a common point (Hauke, 1963).
Among terrestrial plants, only the horsetails have been definitively shown to require Silicon as an essential, not simply beneficial, mineral nutrient (Epstein, 1999). The requirement for silicon has been shown for Equisetum arvense (Chen & Lewin, 1969) and for E. hyemale (Hoffman and Hillson, 1979), so this requirement appears to hold for members of both subgenera within Equisetum.
Golub and Whetmore (1948) excavated the rhizome system of a colony of Equisetum arvense to a depth of 2 m and found five successive horizontal layers of rhizomes connected by vertical rhizomes. This rhizome system extended below 2 m, but the investigators did not excavate further. This "tiered" rhizome architecture may be unique in the plant kingdom. Indeed, other rhizomatous plants generally have but a single horizontal rhizome system layer (Bell & Tomlinson, 1980).
Equisetum is an ancient genus and comprises the sole surviving representatives of the class Sphenopsida (the only class of the subdivision Sphenophytina) (Scagel et al., 1984). Sphenopsids first appeared in the fossil record of the late Devonian. The earliest unequivocal sphenopsid that has been discovered is Pseudobornia ursina, a monopodial arborescent clonal plant of the upper Devonian which grew up to 20 m tall with stems up to 60 cm in diameter (Scagel et al., 1984; Stewart and Rothwell, 1993). Pseudobornia dominated clastic streamside habitats during this time (Behrensmeyer et al. 1992). Later, during the early Carboniferous, a greater diversity of distinctly sphenopsid plants became prominent. These Carboniferous sphenopsids are currently classified into two orders, the Sphenophyllales and the Equisetales (Stewart and Rothwell, 1993). The Sphenophyllales, consisting of a single genus, Sphenophyllum, were herbaceous plants with whorls of wedge-shaped leaves on a jointed stem. Sphenophyllum species increased in abundance until the Upper Carboniferous, but vanished by the end of the Permian. The Equisetales include the major families Archaeocalamitaceae, Calamitaceae, and Equisetacae. The Archaeocalamitaceae were arborescent sphenopsids which persisted from the Upper Devonian through the Lower Permian and were similar to the much more numerous Calamitaceae (Stewart & Rothwell, 1993). The Calamitaceae, which has a single genus, Calamites, encompasses the now extinct arborescent woody sphenopsids, some of which attained heights of up to 30 m and diameters of up to 1 m (Cleal & Thomas, 1999; Scagel et al., 1984, Spatz et al., 1998b). Finally, the family Equisetaceae consists of the living genus Equisetum as well as other extinct herbaceous sphenopsids resembling Equisetum. Interestingly, the Calamitaceae closely resembled the Equisetaceae in having rhizomatous growth, fused leaf sheaths at the nodes, and in many other respects. The chief differences between the two families lie in cone morphology and in the lack of secondary (woody) growth in the Equisetaceae in contrast to the presence of secondary growth in the Calamitaceae (Stewart & Rothwell, 1993).
The Carboniferous represented the peak of pteridophyte diversity and abundance (Rothwell, 1996). It was also during this period that about 75 % of the world's coal was formed. Hence, there is rich fossil evidence for the ecology and biogeography of this period. The great Carboniferous coal swamps were warm and humid and occupied the wet tropical low-lying areas (Pearson, 1995). These swamps were dominated by giant arborescent Lycopods in genera such as Lepidodenderon (Stewart & Rothwell, 1993). Sphenopsids, especially in the genera Calamites and Sphenophyllum were common members of the flora during the Carboniferous. The Pennsylvanian plant assemblages are probably the best known plant assemblages of the Paleozoic, and possibly the entire pre-Cretaceous. From palynological and coal-ball analyses of Pennsylvanian floras, it is possible to gain insight into the ecology of Carboniferous sphenopsids. Sphenophyllum species were ground-cover plants which occurred in nearly all lowland habitats (Behrensmeyer et al., 1992). Calamites were hydrophytes, like Equisetum, and grew on loosely consolidated substrates such as sand bars, lake and stream margins, and other unstable moist substrates (Tiffney, 1985). Therefore, it is probable that Calamites were centered outside the comparatively stable coal swamps. Calamites were the only Carboniferous lowland arborescent plants that had the capability for extensive vegetative propagation (Tiffney, 1985). The rhizomatous growth of Calamites, like that of modern Equisetum, allowed them to form extensive colonies on disturbed wetland areas. However, Calamites and Sphenophyllum were relatively minor components of the vegetation in terms of overall biomass contribution (Behrensmeyer et al., 1992; Tiffney, 1985). The aerial stems of Calamites were of determinate growth, like those of modern horsetails, despite their capacity for secondary xylem formation (Eggert, 1962).
During the Carboniferous, Laurasia and Gondwana collided and thus began the formation of the supercontinent Pangea. In the Late Carboniferous, there was widespread peat formation in the moist equatorial region coal forests in what is now Europe and central and eastern North America. However, climate changes in the late Pennsylvanian and early Permian began to herald the demise of the great coal swamps. During this time, the equatorial regions of Pangea became drier and rainfall became more seasonal (Parrish, 1993). The climate also became cooler with extensive glaciation in the southern hemisphere. This trend continued through the Triassic when arid to semiarid climates prevailed (Stewart and Rothwell, 1993). This led to a worldwide change from hydric conditions to mesic conditions which are less favorable to sphenopsid growth. In addition, the inability of sphenopsids to grow in the increasingly dry sites probably reduced their ability to compete with the increasingly successful ferns, cycads, and conifers (Koske et al., 1985). These changes probably led to the extinction of Calamites during the Lower Permian and the extinction of the Sphenphyllales by the end of the Permian. These extinctions left the remaining members of the Equisetales as the only representatives of the Sphenophytina (Stewart and Rothwell, 1993).
By the Mesozoic, all sphenopsids had the same basic structure as present day Equisetum (Behrensmeyer et al., 1992). The remaining Equisetales included the widespread Schizoneura, an upright herbaceous genus, with stems up to 2 meters tall and 2 cm wide (Behrensmeyer et al., 1992), which first appeared in the Carboniferous and continued into the Jurassic (Stewart and Rothwell, 1993). Schizoneura's large fiat unfused leaves were a distinctive feature of this genus not commonly found in the Equisetales (Scagel et al., 1984). Another herbaceous sphenopsid which survived from the Carboniferous to the Lower Cretaceous was the genus Phyllotheca (Stewart and Rothwell, 1993). In addition, the genus Neocalamites first appeared in the Upper Permian and survived until the Lower Jurassic. Neocalamites resembled a small Calamites in gross morphology (Stewart and Rothwell, 1993) with stems 10 to 30 cm thick and possibly 10 m high (Behrensmeyer et al., 1992). It was widely distributed during the latter Triassic (Seward, 1959). Equisetites, a genus which first appeared in the Carboniferous, was the other major surviving genus of sphenopsids. Equisetites were very similar to present day Equisetum and there is some controversy as to whether they may actually have been congeneric with present day Equisetum. If Equisetites actually were Equisetum, then Equisetum has existed since the Paleozoic and may indeed be the oldest extant vascular plant genus (Hauke, 1963). However, some Triassic and Jurassic Equisetites were significantly larger than present day Equisetum, reaching 8 to 14 cm in diameter (Stewart and Rothwell, 1993). Perhaps the largest Equisetites species, E. arenaceus, lived during the Upper Triassic period (Kelber & van Konijnenburg-van Cittert, 1998). This remarkable species had stems that averaged 25 cm in diameter and may have reached 10 m in height. Stewart and Rothwell (1993) hypothesized that large Equisetites may have had secondary growth due to their size, but mention that there is no direct evidence for this. Seward (1898) mentioned interesting indirect evidence that E. areanceus had secondary growth. Some bamboos have stems approaching the diameter of E. arenaceus, yet lack secondary growth (Judziewicz et al., 1999). Bamboo stems are supported by extensive lignification (Judziewicz et al., 1999) and it seems possible that the large Equisetites likewise had lignified support tissues. Spatz et al. (1998a) did not find lignification in the supporting tissues of giant Equisetum stems. Gierlinger et al. (2008) found E. hyemale stems to be free of lignin, but Speck et al. (1998) reported slight lignification in supporting tissues of the latter species. Yamanaka et al. (2012) found that lignin is present in E. hyemale vascular bundles, but not the outer siliceous layers, and that lignin plays no mechanical role.
The distribution and anatomy of Mesozoic sphenopsids was consistent with primary colonization of open or disturbed moist habitats. The sphenopsids as a whole became less diverse and increasingly limited to herbaceous forms during the Triassic (Behrensmeyer et al., 1992). This trend was probably due to increasingly arid conditions during the Triassic. However, the surviving order Equisetales was widely distributed and diverse during the Mesozoic. During the Jurassic, the large Equisetites were present in nearly all parts of the world. From the Jurassic onwards, however, Equisetales become smaller and less numerous (Schaffner, 1930). The Jurassic has also yielded the earliest definitive fossil species of Equisetum (Channing et al., 2011). By the beginning of the Cenozoic, relatively small species of Equisetum are all that appear (Stewart and Rothwell, 1993). This decrease in size and abundance during the Cretaceous was probably also related to the rapid rise of angiosperms to dominance and the resulting general decline in the prominence of pteridophytes and conifers (Schaffner, 1930). However, despite this decline, during the Quatemary Equisetum species were found to be widely distributed in the temperate zone (Seward, 1959).
Present day Distribution and Species Relationships
Present day Equisetum species are naturally distributed throughout much of the world, although they are notably absent from Australia and New Zealand (Scagel et al., 1984) and from the islands of the central Pacific, Indian, and South Atlantic oceans (Schaffner, 1930). The diversity of species increases from the equator to the temperate zone in the northern hemisphere, whereas there are only four species in the Southern Hemisphere (Hauke, 1963, 1978).
The present day species of the genus Equisetum has traditionally been divided into two distinct subgenera: subgenus Equisetum, with eight species and subgenus Hippochaete, with seven species. However, recent molecular phylogenetics studies have caused a reconsideration of the placement of E. bogotense, once thought to be a member of subgenus Equisetum and even a specialized member of that subgenus (Hauke, 1968, 1969a), but now thought to be either basal to the genus as a whole (Des Marais et al., 2003; Guillon, 2004), or sister to Hippochaete (Guillon, 2007). Due to the ongoing uncertainty about the placement of E. bogotense, the traditional subgeneric names will be retained in this review, with the understanding that intrageneric groupings will likely need to be revised pending further evidence on the placement of this species and pending more comprehensive molecular studies. The placement of E. bogotense aside, the other 14 species make up two sister monophyletic groups in agreement their traditional subgeneric placement. Another surprising finding of molecular phylogenies of Equisetum is the nesting of E. giganteum well within the Hippochaete (Des Marais et al., 2003; Guillon, 2004, 2007), whereas this species had long been considered the basal member of the whole genus based on several macromorphological similarities with fossil taxa such as Equisetites (Hauke, 1963) and bolstered by the apparently unique sexual expression (typically bisexual) of the gametophytes of this species (Hauke, 1969a, 1985), although this character was questioned by Duckett and Pang (1984) based on misidentified experimental plants (Hauke, 1985). Browne (1920) did not find any clear evidence that E. giganteum exhibits any vascular characters that would ally it with Equisetites, but Browne (1922) did find some vascular features she considered basal within the genus, although this interpretation was not clearcut. However, study of the rhizome anatomy did not reveal clear differences with other members of the genus (Browne, 1925). Likewise, recent studies of strobilus structure and ontogeny in E. giganteum suggest no substantial differences with other Equisetum (Rincon et al., 2011).
There are several primary differences between the two subgenera. Species in subgenus Equisetum have stomata that are flush with the epidermal surface, whereas members of the subgenus Hippochaete have stomata that are sunken below the epidermal surface. Stems of subgenus Equisetum are short-lived, relatively sot, and tend to be regularly branched, whereas stems of the subgenus Hippochaete, with few exceptions, tend to be long-lived, hard, fibrous, and unbranched or irregularly branched (Hauke, 1963, 1969b). In addition, four of the species of subgenus Equisetum demonstrate stem dimorphism between non-photosynthetic, unbranched, coniferous stems and photosynthetic, branched, vegetative stems (Hauke, 1978). No such dimorphism occurs in the subgenus Hippochaete (Hauke, 1963). Although the chromosome number (n= 108) is the same for all Equisetum species, the subgenus Hippochaete has larger chromosomes than those of subgenus Equisetum (Hauke, 1978).
The subgenus Hippochaete includes the Equisetum species often called "scouring rushes" (although also known generally as horsetails) due to their rough, silica-impregnated epidermis. The rough siliceous stems of plants of this subgenus were used by American pioneer settlers for scouring dirty cookware and polishing wood (Scagel et al., 1984). The seven species in this group are E. giganteum, E. myriochaetum, E. ramosissimum, E. laevigatum, E. hyemale, E. variegatum and E. scirpoides. This group contains the two largest Equisetum species, E. giganteum and E. myriochaetum. With the exception of E. laevigatum, and some varieties of E. ramosissimum, all of the species in this subgenus have evergreen stems (Hauke, 1963). This group is very widespread with species distributed over large areas of every continent, except for Australia and New Zealand. The Old World species E. ramosissimum, which ranges from 60[degrees] North latitude to 30[degrees] South latitude, has the widest latitudinal range of any Equisetum species (Schaffner, 1930). The subgenus Hippochaete, as a whole, ranges as far north as Ellesmere Island (greater than 80[degrees] North latitude) and as far south as Argentina (approximately 40[degrees] South latitude) (Hauke, 1963).
The subgenus Equisetum contains the species commonly known as "horsetails." The eight species of this group are E. arvense, E. pratense, E. sylvaticum, E. fluviatile, E. palustre, E. diffusum, and E. telmateia. The species in this group tend to be regularly branched. Members of this subgenus are found from 80[degrees] North latitude to 40[degrees] South latitude. No species in this subgenus extends into the Southern Hemisphere. The other seven species of this group are found in the Northern Hemisphere (Hauke, 1963). Most species of subgenus Equisetum are temperate, with a few extending their ranges into the subtropics and only E. bogotense ranging into the tropics. The aerial stems of all of these species, except for E. bogotense and E. diffusum, (the species from the warmest climates), are annual (Hauke, 1978).
Equisetum species grow in wet places such as moist woods, ditches, wetlands, and in road fill where sufficient groundwater is available. Rhizomatous clonal growth is a universal feature of the genus and is very important in its ecology and its ability to utilize ground water. A single rhizome system may cover hundreds of square feet (Hauke, 1963). The rhizomes can penetrate to soil depths of four meters in some circumstances (Page, 1997). This deep rhizome growth gives the plants the ability to survive environmental disturbances such as plowing, burial, fire and drought. The extensive rhizome system also allows the Equisetum plants to supply themselves with water and mineral nutrients from deep underground and hence allows them to grow in habitats, such as road fill, which appear dry on the surface (Hauke, 1963).
As in other pteridophytes, sexual dispersal in Equisetum occurs by means of spores. Equisetum spores are green, spherical, and have thin spore walls (Hauke, 1963). Each Equisetum spore has four unique strap-like structures called elaters attached to the spore surface at a common point. These elaters are hygroscopic (i.e. they expand and contract with changes in humidity) and probably function to help disperse the spores (Hauke, 1963). Equisetum spores are short-lived and can germinate within 24 h of release from the cone. After 5-17 days, depending on humidity, they are no longer capable of germination (Hauke, 1963), although very cold storage temperatures can extend viability to 2 years or more (Ballesteros et al., 2011). In non-tropical species (the majority of Equisetum), the spores are produced over a short period of time during the growing season (Duckett, 1985). Equisetum gametophytes appear to require a substrate of recently exposed bare mud in order to become established (Duckett & Duckett, 1980). The two subgenera tend to have consistent differences in their gametophytes, with those of the Hippochaete being considerably larger and having more embryos than those of subgenus Equisetum (Campbell, 1928), sometimes reaching 3.5 cm in diameter (Mesler & Lu, 1977). However, form and sexuality can be plastic in response to environmental differences (Walker, 1931; Buchtein, 1887; Mesler & Lu, 1977). Like pioneer species, they rapidly attain sexual maturity and are adversely affected by competition from bryophytes and vascular plants (Duckett & Duckett, 1980; Duckett, 1985). The resulting inefficiency of spore germination and gametophyte reproduction in non-pioneer situations probably limits gene flow and leads the high degree of genetic divergence found between Equisetum populations (Korpelainen & Kolkkala, 1996). Therefore, sexual reproduction in Equisetum is limited to rather narrow ecological conditions and this limits the establishment of Equisetum via spores.
The uniform chromosome number throughout the genus (n= 108) facilitates hybridization between Equisetum species (Scagel et al., 1984). Hybridization is also favored by the relatively narrow ecological requirements of gametophytes which encourages the formation of mixed populations of gametophytes on suitable sites (Hauke, 1978). These mixed populations increase the probability of cross fertilization between gametophytes of different, but compatible, species. In areas where environmental conditions are especially conducive to spore germination and gametophyte establishment, Equisetum hybrids are particularly frequent and widespread. In Britain and Ireland, for example, Equisetum hybrids are particularly successful (Page, 1985). This success appears to be due primarily to the moist temperate oceanic climate and relatively low competition from other plants, conditions which favor both gametophyte and sporophyte generations of Equisetum (Page, 1985). Equisetum hybridization is especially frequent within the subgenus Hippochaete where five common hybrids are known. Within the subgenus Equisetum, there is only one common hybrid (Hauke, 1978) and the most common species involved in hybridization is E. arvense (Lubienski, 2010). There are many more known hybrids within each subgenus, but these hybrids tend to be much less common (Hauke, 1978). No hybrids between the two subgenera have yet been reported and this adds further evidence that the two subgenera are naturally distinct (Krahulec et al., 1996). Furthermore, there are no known hybrids of the enigmatic Equisetum bogotense, though this may be partly due to its lack of distributional overlap with any species besides the giant horsetails. Use of ISSR fingerprinting has facilitated identification and verification of hybrids (Brune et al., 2008).
Several triploid taxa have been discovered in subgenus Hippochaetae, either the result of introgression within hybrids or of crossing of a gametophyte from an unreduced spore of one species and a normal gamete from another species (Bennert et al., 2005; Lubienski et al., 2010). Tetraploids are unknown (Bennert et al., 2005).
Equisetum species have a remarkable ability to reproduce vegetatively. This mode of reproduction predominates in some species (e.g. E. arvense), whereas others reproduce sexually with greater frequency (e.g. E. telmateia) (Brune et al., 2008). Vegetative reproduction helps to compensate for the inefficiency of spore reproduction. An extensive rhizome system allows Equisetum species to rapidly colonize disturbed areas (Hauke, 1963). This ability gives Equisetum a distinct advantage over species requiring seed establishment or which have slow-growing rhizomes (Hauke, 1969b). For instance, the widespread creation of roadside ditches in America has created significant new habitat for some Equisetum species. This is because the soil in ditch habitats tends to be moist and the rhizomatous growth of Equisetum species allows them to survive and thrive under the conditions of sediment accumulation that are characteristic of ditches (Rutz and Farrar, 1984). The ability of Equisetum to survive and spread in areas of heavy sediment accumulation was dramatically demonstrated after the 1912 eruption of Katmai Volcano in Alaska. In studies of vegetational recovery from the volcanic tephra (ash and silt) deposited by this eruption, E. arvense was found to be the most successful herb. It was able to penetrate as much as one meter of tephra, more than any other herbaceous species, and colonize large areas via rapid rhizomatous growth (Bilderback, 1987). The remarkable ability of Equisetum to prosper under disturbed conditions was also demonstrated after the eruption of Mount St. Helens in 1980 when Equisetum formed almost monotypic stands in the newly deposited tephra (Siegel & Siegel, 1982; Rothwell, 1996). The deep rhizome system of Equisetum also allows these plants to survive fire and rapidly recolonize burned-over sites (Beasleigh & Yarranton, 1974). It is probable that the vigorous and extensive rhizomatous habit of Equisetum has been very important to the long term survival and spread of the genus (Hauke, 1969b).
Fragmentation of rhizomes and stems allows Equisetum to disperse readily in suitable habitats where there is sufficient moisture. Even the aerial stem fragments can sprout and form new colonies (Praeger, 1934; Schaffner, 1931; Wagner & Hammitt, 1970). Some members of the subgenus Equisetum (e.g. E. arvense and E. palustre) also reproduce vegetatively via tubers produced on the rhizomes (Hauke, 1978). These tubers can contribute substantially to vegetative spread through soil disturbance (Marshall, 1986; Sakamaki and Ino, 2006). Hence, vegetative reproduction allows Equisetum clones to persist and spread even in the absence of sexual reproduction (Hauke, 1963).
Vegetative reproduction probably accounts for the widespread occurrence and persistence of common Equisetum hybrids even where one or both of the parents are absent. This is because hybrids are generally sterile and hence are without means of sexual reproduction. The rhizome system of a vigorous hybrid clone theoretically has the ability to maintain dense colonies within limited areas for long periods. Fragmentation and transport of rhizomes and stems then has the potential to disperse the clone from the site of the original hybridization. This would account for the abundance of Equisetum hybrids even if hybridization is a relatively uncommon occurrence (Hauke, 1963).
Spatz et al. (1998a) studied the biomechanics of a giant horsetail, Equisetum giganteum. The investigators found that E. giganteum has a turgor-based support structure that is distinct from the lignification-based support found in hollow-stemmed grasses. The results of the study demonstrated stems taller than ~2.0-2.5 m were not mechanically stable (i.e. they buckle without external support). Taller stems required support of neighboring stems (facilitated by intertwined side branches) to remain upright. The stems of the clone they studied were relatively thin, only reaching ~1 cm at the widest. Husby (2009) studied the biomechanical properties of E. giganteum stems in the field in southern South America. The bulk tissue modulus of elasticity values measured on wild-grown stems were much higher than those measured by Spatz et al. (1998a). This finding, along with larger maximum diameters (~3.9 cm) of field grown plants explains the significantly taller (5+ m) stems found in the wild.
Speck et al. (1998) found that another member of the subgenus Hippochaete, E. hyemale, had some biomechanical properties quite distinct from those of the E. giganteum that Spatz et al. (1998a) studied. In E. hyemale, stem stability is not turgor dependent, but is primarily attained through the arrangement of two endodermis layers and a hypodermal sterome. Equisetum hyemale is primarily a cold-climate species (Hauke, 1963), and stems remain evergreen and functional for multiple seasons (Niklas, 1989a). During subfreezing temperatures, E. hyemale has the ability to dehydrate its tissues via extracellular freezing to avoid ice crystal damage to tissue (Niklas, 1989a). The non-turgor-dependent structure of E. hyemale thus permits the stems of this species to avoid buckling even when turgor pressure is decreased during winter. The nodal septa of E. hyemale shoots contributed 17 to 32 % of the flexural rigidity of the axes (Niklas, 1989b). Furthermore Niklas (1989c) found that the stems of E. hyemale are primarily designed for mechanical stability, rather than economy of tissue allocation.
Spatz et al. (1998b) combined the mechanical properties of extant Equisetum with insights from the arborescent Paleozoic genus Calamites which has a very similar stelar structure to Equisetum (Verdoorn, 1938) to model the biomechanical properties of the latter. The maximum heights of Calamites stems in exposed areas were likely limited by wind stresses. In addition, like E. hyemale, but in contrast to E. giganteum, Calamites appears to have had a non-turgor-dependent reinforcing structure.
Treitel (1943) carried out experiments on the rhizome hiomechanics of several Equisetum species from both subgenus Hippochaete and subgenus Equisetum. He investigated rhizome elasticity, breaking stress, and breaking strain. The results of the study indicated that different Equisetum species often had markedly different stress-strain curves. The investigator attributed these differences to differences in amount of strengthening elements in rhizomes (e.g. suberization and schlerenchyma cells) that are in turn due to differences in soil environment (wetter vs. drier soil) and to rhizome maturity. The two species for which Treitel calculated the modulus of elasticity had very different values of this parameter, with E. fluviatile (subgenus Equisetum) having much more elastic rhizomes than E. scirpoides (subgenus Hippochaete). He attributed E. fluviatile's greater elastiscity to its much wetter habitat and hence its lesser need for strengthening tissues to reinforce its rhizomes against soil pressure.
David et al. (1990) observed a marked water potential depression in Equisetum telmateia around noon even when vapor pressure deficit was relatively mild, despite the presence of a high surface water table. This suggests that either water transport or root absorption, or both, were unable to keep up with evaporative demand during those periods. Also, Husby (2009) observed low maximum stomatal conductance in Equisetum giganteum. Since hydraulic conductivity is generally closely correlated with stomatal conductance (Franks & Brodribb, 2005), it appears likely that there exist hydraulic "bottlenecks" at the nodes in Equisetum stems that limit water transport sufficiently to reduce stomatal conductance. The carinal canals are not continuous through the nodes (Gifford & Foster, 1989), which likely increases resistance to water flow. These observations suggest that hydraulic conductivity is a limiting factor for modern horsetails, even thought their evaporative surface area is decreased by the absence of exposed leafly lamina.
The hydraulic architecture of Equisetum stems has yet to be elucidated, although the carinal canals in each internode appear to provide low resistance pathways through internodes, analogous to the role played by vessels in angiosperms (Leroux et al., 2011; Xia et al., 1993; Bierhorst, 1958). Such a function would have particular importance during internode elongation when xylem pathways are not yet functional (Leroux et al., 2011). Furthermore, Leroux et al. (2011) discovered a distinctive cell wall matrix lining the carinal canals, which may function to facilitate water transport. Husby (2009) observed that young stems guttate much more readily and show less sensitivity of stomatal conductance to environmental factors than do mature stems, which may be indicative of differences in water transport physiology. There is also evidence that some species of Equisetum transpire much more than others, with the most hydrophilic species, E. fluviatile, showing the highest transpiration rates (Dosdall, 1919). Investigation of water transport physiology for a variety of ecologically distinct Equisetum species would likely yield interesting insights.
Hydathodes and Guttation
Equisetum species, like many other plants, have hydathodes (Johnson, 1936). In Equisetum, these are structures that are associated with veins on the leaf and/or sheath (Johnson, 1936) and serve as exit routes for xylem water when there is positive hydrostatic pressure (called root pressure) in the xylem (Nobel, 1999). The exit of this xylem water, termed guttation, results in the formation of small droplets in the vicinity of the hydathodes. Guttation occurs when transpiration is nil, such as under very high relative humidity conditions or at night (Nobel, 1999) (Fig. 1e). This phenomenon may serve to prevent flooding of mesophyll tissue in leaves (Johnson, 1936). Johnson (1936) studied the anatomy of hydathodes in many Equisetum species and noted that the hydathodes of E. giganteum are "confined to the leaf and sheath bases."
Soil and Root Interactions
Adventitious Rooting as an Adaptation to Disturbance
All equiseta have pre-formed bud and root primordia at each node of both the aerial stems and underground rhizomes (Gifford & Foster, 1989). This allows Equisetum stems to quickly put forth new roots and shoots on aerial stems when the stems are partly or wholly buried in sediment. Hence, even if the deeper parts of a stem or rhizome become crushed or smothered by sediment, the upper parts may be able to survive and reestablish the clone (Gastaldo, 1992). This ability is clearly advantageous for enhancing survival of Equisetum species in the wake of disturbance events in riparian and other wetland habitats. The pre-formed primordia can also facilitate vegetative propagation and dispersal via stem pieces (Wagner & Hammitt, 1970; Hauke, 1963). Schaffner (1931) and Praeger (1934) utilized the adventitious rooting capabilities of Equisetum stems to successfully propagate many species from aerial stem cuttings.
Gastaldo (1992) gives evidence for similar stem regeneration abilities in the large extinct Equisetum relative Calamites and discusses the ecological importance of these abilities. Similarly, Kelber & van Konijnenburg-van Cittert (1998) found that the extinct close relative of extant horsetails, Equisetites arenaceus, could propagate vegetatively via the adventitious rooting of shed branches.
Adaptations to Waterlogged Soil
Like nearly all organisms, plants require oxygen ([O.sub.2]) for efficient cellular respiration. Plants that grow in water-saturated soil often have to cope with anoxic conditions around their underground organs (Blom and Voesenek, 1995). This is because [O.sub.2] diffuses 10,000 times more slowly through liquid water than through air (Grable, 1966). Under waterlogged conditions, cellular respiration by plant roots and soil microorganisms often quickly depletes the available [O.sub.2], leading to anoxic soil conditions (Drew & Lynch, 1980; Kludze & DeLaune, 1995). These conditions lead to a large decrease in plant nutrient availability (Ernst, 1990) and to buildup of phytotoxins produced by anaerbic soil mierobes or by anaerobie respiration in plant roots (Koch & Mendellsohn, 1989).
To deal with anoxic conditions, wetland plants have several morphological and physiological adaptations to maintain aerobic respiration by facilitating transport of [O.sub.2] from the atmosphere to underground and underwater organs (Allen, 1997). In many wetland plants, gas spaces (lacunae) in specialized tissue (called aerenchyma) provide pathways for [O.sub.2] and carbon dioxide (C[O.sub.2]) to move from one part of the plant to another much more quickly than would be possible through tissue without lacunae (Allen, 1977). Rhizomes and stems of wetland Equisetum species have large canals that are thought to function like aerenchyma tissue in facilitating [O.sub.2] transport (Hauke, 1963; Hyvonen et al., 1998). Oxygen movement through aerenchyma occurs either by diffusion alone or by diffusion combined with convection (Allen, 1997). These mechanisms and their relative effectiveness have many important implications both for wetland ecology and for the growth and productivity of crop plants, such as rice (Oryza sativa L.), that typically grow in waterlogged soils (Allen, 1997; Wassmann & Aulakh, 2000). The most efficient known mechanism for oxygen transport to submerged plant parts is via pressurized convection (Allen, 1997).
Until very recently, studies of pressurized [O.sub.2] transport in wetland plants have focused exclusively on angiosperms, with the exception of one study that investigated the gymnosperm Taxodium distichum L. (Grosse et al., 1992). However, the rhizomes of Equisetum species often concentrate more deeply than the roots and rhizomes of accompanying vegetation (Borg, 1971). Marsh et al. (2000) found that, in an Alaska wetland Equisetum rhizomes were concentrated in the deeper C soil horizon whereas the roots and rhizomes of other species were concentrated in the surface O horizon. The especially deep penetration of waterlogged sediments by Equisetum rhizomes suggests the existence of efficient mechanisms for rhizome aeration, Page (2002) mentioned that Equisetum species in the British Isles vary in their tolerance of anaerobic soil water conditions. Equisetum fluviatile appears able to tolerate the greatest degree hypoxia in soil water whereas E. telmateia is least tolerant of anaerobic soil water and occupies sites with continually flowing groundwater.
The first studies of gas transport in Equisetum dealt with E. fluviatile, a species that frequently grows as an emergent aquatic plant (Hauke, 1978) and one of the most anaerobiosis tolerant Equisetum species (Page, 2002). An early study by Barber (1961) found a diffusion gradient from high concentrations of [O.sub.2] and low concentrations of C[O.sub.2] in aerial stems to the inverse condition in submerged rhizomes. In addition, Barber (1961) found that diffusion along excised aerial stems was relatively efficient. However, this study did not provide information that would indicate whether or not a pressurized ventilation mechanism might be active in E. fluviatile. A study by Hyvonen et al. (1998) of methane release from an E. fluviatile stand suggested that this species does not have a pressurized ventilation flow system because there was not a discernable diurnal pattern of methane efflux. Similarly, Strand (2002) found that E. fluviatile had a "low or non-detectable" air flow rate in its stems, yet was found in "unexpectedly deep water".
Two recent studies have found surprisingly high rates of pressurized ventilation in some Equisetum species. Armstrong and Armstrong (2009) found the first clear case of substantial pressurized ventilation in a nonflowering plant, Equisetum telmateia. In fact, the ventilation rates discovered in this plant were higher than any rates recorded in angiosperms, including the giant water lily, Victoria amazonica. The relevant features of Calamites stem structure (e.g. stomatal structure and stem anatomy) are similar to those of E. telmateia, suggesting that this ancient genus may also have tolerated waterlogged soils via pressurized ventilation.
However, not all Equisetum species exhibit pressurized ventilation. Only species with cortical araenchyma that is interconnected among the branches, aerial shoots and rhizomes exhibited convection (Armstrong and Armstrong, 2010). Nine horsetail species were studied, but only four exhibited pressurized convection, including species from both subgenera. Stomatal behavior also played a role in the differences. Whether the gas flow channels within Equisetum shoots and rhizomes allow for refixation of C[O.sub.2] respired underground remains to be investigated (Raven, 2009).
Soil Preferences and Nutrient Cycling
Alvarez de Zayas (1982) observed that in Cuba Equisetum giganteum is associated with mineral rich, acidic, alluvial soils. Correspondingly, recent experience with Equisetum in cultivation suggests that they have a high requirement for some micronutrients (C. Husby, unpublished observation). However, some species are capable of tolerating and even dominating nutrient poor environments (Sarvala et al., 1982)
Equisetum tissue is frequently observed to be rich in the minerals P, K, Ca, magnesium (Mg), and silicon (Si) (Auclair, 1979; Marsh et al., 2000; Pulliainen & Tunkkari, 1991; Saint Paul, 1979; Thomas & Prevett, 1982). Andersson (1999a, b) showed experimentally that E. arvense has a high K demand under high light conditions and was able to tolerate lower N levels (although its inability to respond much to increased N availability renders it vulernable to being out-competed by faster growing plants). Furthermore, certain Equisetum species have been shown to be highly nutritious for wildlife. For example, young stems of E. fluviatile can contain more than 20 % protein along with sufficiently high levels of P, K, Ca and Mg to meet the mineral needs of breeding geese and their young (Thomas and Prevett, 1982). In some areas, Equisetum species are an important part of the diet of black bears (Machutchon, 1989), voles (Holisova, 1976; Jean & Bergeron, 1986), rock ptarmigan (Emison & White, 1988), young trumpeter swans (Grant et al., 1994) and fish (Brabrand, 1985). Hauke (1969b) observed that cattle in Costa Rica appear to relish giant horsetails and one rancher believed that his cattle benefited from eating it.
Members of the genus Equisetum have the ability to extend their rhizomes deeply into saturated soil (Borg, 1971 ; Marsh et al., 2000). The rhizome system has generally been found to comprise most of the plant's biomass (Borg, 1971; Marshall, 1986). The ability of Equisetum rhizomes to penetrate deeply into wetland soils plays an important part in their recently discovered role as nutrient pumps. In an Alaskan shrub wetland, Marsh et al. (2000) found that Equisetum species can acquire and accumulate substantial amounts of phosphorus (P), potassium (K), and calcium (Ca) from lower soil layers and transport these nutrients to the surface where they are available to other plants. Remarkably, these investigators found that, although Equisetum species made up only 5 % of the total biomass of the wetland community, the Equisetum tissues had 16 % of the total phosphorus and 24 % of the total potassium (Marsh et al., 2000). Furthermore, Equisetum species contributed disproportionately to soil nutrient inputs in the shrub wetland. During the two year study period, Equisetum litter provided 75 % of the calcium, 55 % of the phosphorus, and 41% of the K input to the soil (Marsh et al., 2000). The nutrient pumping of Equisetum species in the shrub wetland probably contributed to the unusually high primary productivity of the ecosystem (Marsh et al., 2000). This nutrient pumping function of the shrub wetland Equisetum species appears to be at least partly due to the ability of Equisetum rhizomes and roots to penetrate more deeply into the soil than roots and rhizomes of other wetland plants. While Equisetum roots and rhizomes were concentrated in the deeper C horizon of the soil, roots and rhizomes of other wetland plants concentrated in the surface O horizon (Marsh et al., 2000).
A remarkable characteristic of Equisetum species is their ability to take up and accumulate silicon in their tissues. The resulting silicon concentrations in Equisetum stems are the highest among vascular plants, but lower than liverworts (Hodson et al., 2005). Silica accumulates on the epidermis of the plants (Parsons & Cuthbertson, 1992; Sapei et al., 2007). It is also incorporated into the cell walls, perhaps crosslinking wall polymers and increasing their rigidity and stability (Currie & Perry, 2009). Research on the protective value of silica seems to indicate that silica solutions when applied to plants can provide effective protection from fungal diseases and from insect attack (Epstein, 1999). This would explain why gardeners have long used horsetail extract to protect plants against pathogens and predators (Quarles, 1995). The outer layer of silica on Equisetum stems may help explain why horsetails appear to be little bothered by insect feeding or fungal diseases (Hauke, 1969b; Kaufman et al., 1971). This outer layer may also help reduce water loss through the epidermis (Kaufman et al., 1971).
Timell (1964 found that silicic acid content of E. palustre could reach 25.3 % of dry weight. An important function of cell wall silica in Equisetum is in maintenance of shoot erectness (Kaufman et al., 1971) as an alternative to lignin (Siegel, 1968; Yamanaka et al., 2012). Furthermore, silica content of stems appears to be directly associated with stem longevity (Srinivasan et al., 1979). Horsetails incorporate much silicon into their stem tissues and external ridges, knobs, and rosettes of silicon give the stems of many species their rough and abrasive character (Gifford & Foster, 1989; Hauke, 1963). People have taken advantage of this abrasive quality by using Equisetum stems to wash dishes (hence the common names 'scouring rush' and 'limpiaplata'), polish woodwind reeds, and polish silver (whence the name 'yerba del platero' in Argentina).
Mycorrhizae and Root Hairs
Until recently, there has been little convincing evidence of mycotrophy in Equisetum species (either in the gametophyte or the sporophyte stage) and most studies have found essentially no mycorrhizal colonization of horsetails (Read et al., 2000). Although Koske et al. (1985) found fungal structures in roots of Equisetum species growing in a sand dune habitat, the close association of the Equisetum roots with roots of characteristically mycotrophic plants raised the possibility that the observed fungal structures represented "simply the penetration [of Equisetum roots by] a 'non-host" (Read et al., 2000). Hence, the role of mycorrhizae in Equisetum ecology remains controversial. Overall, however, Equisetum species clearly appear to do quite well in many situations without mycorrhizal associations (Read et al., 2000). For example, Marsh et al. (2000) found no mycorrhizal colonization of Equisetum roots in the Alaskan shrub wetland they studied. Although enhanced phosphorus acquisition is often a major contribution of mycorrhizal associations to plant nutrition (Orcutt and Nilsen, 2000), the mycorrhizae-free Equisetum species studied by Marsh et al. (2000) absorbed soil nutrients, including phosphorus, very effectively. A recent study of Equisetum bogotense in Argentinian Patagonia produced evidence of falcultative mycotrophy (some individuals were mycorrhizal and others were not) (Fernandez et al., 2008). By contrast, relatively high rates of colonization were found for plants growing at the northern extreme of the genus' distribution on Ellesmere Island (82[degrees]N) in the Canadian Arctic, although non-mycorrhizal plants were also found, indicating once again that the relationship is facultative (Hodson et al., 2009). The authors of this study suggest that previous negative findings may have been primarily due to the lack of adequately sensitive equipment that allows detection of very fine mycorrhizae that accounted for most of the endophyte abundance in the arctic samples.
Schaffner (1938) and Page (2002) have observed that Equisetum species have exceptionally long root hairs and Page (2002) has noted that these hairs are "unusually persistent", at least in water culture. Page (2002) hypothesized that these root hairs may function to enhance the absorptive capacity of Equisetum roots in a manner similar to mycorrhizae. Marsh et al. (2000) noted the presence of root hairs on Equisetum roots in the O horizon but not on roots in the C horizon of the Alaskan shrub wetland they studied. The investigators hypothesized that nutrient concentrations were lower in the O horizon, necessitating greater roots surface area for absorption, whereas nutrient concentrations were high enough in the C horizon to inhibit formation of root hairs. However, this phenomenon may also have been due to lower oxygen availability suppressing root hair formation deeper in the soil.
Uchino et al. (1984) found evidence for high rates of nitrogen fixation activity (attributed to several strains of Enterobacteriaceae) in association with rhizomes and roots of several temperate Equisetum species (two from each subgenus). This was based on measurements of acetylene reduction activity. These investigators hypothesized that association of Equisetum species with nitrogen-fixing bacteria may help horsetails survive in the nitrogen-limited habitats where they frequently grow.
Salinity and Heavy Metal Tolerance
Horsetails are known to tolerate stressful soil environments and this ability appears to extend all the way back to the Jurassic, where Equisetum thermale inhabited a geothermal environment likely characterized by high levels of mercury, arsenic and other elements that tend to be phytotoxic (Channing et al., 2011). Modern Equisetum are also tolerant of heavy metal uptake (Hozhina et al., 2001; Siegel et al., 1985) and have even been used for gold bioprospecting (Brooks et al., 1981).
In some areas Equisetum species grow in saline wetlands. They are sometimes found in association with saline lakes (Williams, 1991) coastal dune slacks (Van der Hagen et al., 2008) and saline boreal wetlands (Purdy et al., 2005).
Page (1997) discussed isolated colonies of the hybrid horsetail, Equisetum x moorei, on the southeast coast of Ireland. These colonies, which are the only known populations of this hybrid in the British Isles, are on dunes and grow quite near to the high tide line, suggesting considerable exposure to saline soil water and salt spray. Interestingly, only one parent, E. hyemale, of this hybrid is present in the British Isles. However, both the other parent, E. ramossisimum, and other populations of E. x moorei are present on the European mainland. These facts lead naturally to the hypothesis that sterile E. x moorei arrived in Ireland via vegetative propagules, such as stem pieces or rhizomes, that may have floated to Ireland from the mainland. Page (1997) noted an experiment (unpublished) with this hybrid wherein cut stem pieces were floated in seawater for various lengths of time and their ability to re-sprout was evaluated. Remarkably, immersion for up to 10 days in seawater did not reduce the ability of stems to sprout roots and form new plants.
Husby et al. (2011) documented a substantial degree of salinity tolerance in E. giganteum populations growing in river valleys in the Atacama Desert in northern Chile. Some of the populations in this area grow close to the ocean where the groundwater they access is up to 50 % of ocean water salinity. Like many other salt tolerant plants, E. giganteum exhibits an ability to exclude sodium and preferentially accumulate potassium under high salinity conditions.
Equisetum species, like many angiosperms, appear to exhibit allelopathy. Milton and Duckett (1985) found that sporophytes of E. sylvaticum inhibit gametophyte development of that species. Furthermore, the same investigators round that water extracts from several Equisetum species reduced the germination of grass seedlings. Two of the three species studied were members of the subgenus Equisetum (E. arvense and E. palustre) and one was a member of the subgenus Hippochaete (E. variegatum). The inibitory effects of the members of the subgenus Equisetum were greater than that of E. variegatum. This suggests that members of the subgenus Hippochaete, and hence the giant equiseta, may be less allelopathic than members of the subgenus Equisetum.
The Giant Horsetails
The giant horsetails are of special interest within the genus Equisetum because they give the closest approximation among living plants to the large stature once attained by primeval Sphenopsids (Fig. 1f). Furthermore, because the giant horsetails inhabit the tropics, they provide insights into how Equisetum has adapted to the challenges of living in tropical ecosystems, in contrast to the majority of species which are temperate. As for all equiseta, the giant horsetails spread vegetatively via extensive rhizome systems, often forming large clones. The rhizomes give rise to erect, determinate, aerial stems that produce regular whorls of lateral branches, giving the stems a remarkably precise radial symmetry. Colonies of such stems have a remarkably ancient appearance, as the 19th century botanist Richard Spruce (1908) remarked upon seeing a grove of giant horsetails for the first time:
"But the most remarkable plant in the forest of Canelos is a gigantic Equisetum, 20 ft high, and the stem nearly as thick as the wrist! ... It extends for a distance of a mile on a plain bordering the Pastasa, but elevated some 200 ft above it, where at every few steps one sinks over the knees in black, white, and red mud. A wood of young larches may give you an idea of its appearance. I have never seen anything which so much astonished me. I could almost fancy myself in some primeval forest of Calamites, and if some gigantic Saurian had suddenly appeared, crushing its way among the succulent stems, my surprise could hardly have been increased. I could find no fruit, so that whether it be terminal, as in E. giganteum, or radical, as in E. fluviatile, is still doubtful, and for this reason I took no specimens at the time, though I shall make a point of gathering it in any state" (Spruce, 1908)
Giant horsetails inhabit elevations between 150 and 3000 m and their distributions tend to follow mountain ranges in the tropics (but not at the southern end of the range of E. giganteum, which reaches temperate southern latitudes). Like other Equisetum species, giant horsetails grow in areas with ample groundwater supply, often along rivers and in wetlands (Hauke, 1963, 1969b). Equisetum giganteum in particular exhibits several morphological features that appear to tie it with its fossil progenitors such as Equisetites: cones borne on lateral branches (Fig. 1g), large size, and sheath teeth (Hauke, 1963).
Although giant horsetails are of considerable botanical interest, relatively little is known about these remarkable plants beyond their taxonomy and anatomy. Indeed, most papers that have dealt specifically with giant horsetail ecology were limited to some qualitative (but intriguing) observations on their natural history (Alvarez de Zayas, 1982; Hauke, 1969b). Although a recent study dealt with quantitative aspects of ecophysiology of E. giganteum (Husby et al., 2011). Two studies have investigated the biomechanics of aerial stems in E. giganteum (Spatz et al., 1998a; Husby et al., in review).
The most extensively studied aspects of the giant horsetails has been their medicinal properties. The medicinal use of giant horsetails has a history that reaches back to the Inca of Peru (Tryon, 1959) and the plants are currently used in medicine (often as diuretics, but also for many other medicinal purposes) throughout Latin America (Gorzalczany et al., 1999; Hauke, 1967; Morton, 1981; Murillo, 1983). Investigators using animal models have found that giant horsetail extracts have diuretic (Gutierrez et al., 1985) and hypoglycemic (Cetto et al., 2000) effects and have "nerve growth factor (NGF)-potentiating activity" (Li et al., 1999). Furthermore, a controlled study by Revilla (2002) showed that traditionally prepared Equisetum myriochaetum extract had significant hypoglycemic effect (not resulting from increased insulin secretion) in type 2 diabetics.
The taxonomy of the giant horsetails gives a good example of the typical means of distinguishing species and hybrids within Equisetum. Taxonomists currently recognize two species of giant horsetail and a hybrid between them: Equisetum giganteum L., E. myriochaetum Schlecht. and Cham., and E. x schaffneri Milde (E. giganteum x E. myriochaetum) (Hauke, 1963). Prior to Hauke's (1963) work, taxonomists recognized a relatively large number of species and varieties of giant horsetails. For example, Milde, in his 1867 monograph of Equisetum, recognized seven species of giant horsetails.
The giant horsetails are some of the least known of the 15 species in the genus Equisetum. All of the giant horsetails are members of the subgenus Hippochaete within the genus Equisetum. Most of the seven members of the subgenus Hippochaete, including the giant horsetails and the familiar temperate "scouring rush", E. hyemale, have tough evergreen stems. However, the giant horsetails are the only Equisetum species that have stems that are both evergreen and regularly (i.e. radially symmetrically) branched. Furthermore, the regular branching habit of the giant horsetails is unique in the subgenus Hippochaete (Hauke, 1963, 1978).
Because the three giant horsetails appear similar in overall habit, and because Equisetum species exhibit considerable morphological plasticity (Hauke, 1963; Schaffner, 1928) (Fig. 1h), more stable anatomical characters are used to distinguish the species (Table 1). The most important diagnostic characters (branch ridge patterns, stomatal patterns, and endodermal patterns) can only be observed under high magnification and many of characters of E. x schaffneri overlap with its parent species (Hauke, 1963). Therefore, accurate identification of giant horsetails can be problematic. As a result, both dried specimens in herbaria (Stolze, 1983; Husby, personal observation) and living specimens in botanical gardens (Moyroud, 1991; Husby, personal observation) are often misidentified.
Giant horsetails are pioneer (early-successional) obligate wetland plants and are poor competitors (Hauke, 1969b). Abundance of groundwater supply and lack of competition are key habitat requirements of these plants. Hence, they are often associated with rivers and alluvial soils (Hauke, 1969b; Alvarez de Zayas, 1982). The limitation of giant horsetails to higher altitudes in the tropics is probably due to their poor competitive abilities and their inability to tolerate shade. Hauke (1969b) observed that the giant horsetails stop producing cones when shaded by other vegetation and are subsequently displaced by other plants. Hence, giant horsetails do not tend to persist in a given site unless the disturbance regime or other factor prevents shading-out of colonies. The lower competitive pressure in the cooler high altitudes combined with increased light intensity may allow the horsetails to "hold their own" against other vegetation (Hauke, 1969b). This would explain why the genus is absent from the lowland Amazon basin where temperatures are warm and plant competition is especially intense. However, E. giganteum grows down to nearly sea level in northern and central Chile where competition is much less (C. Husby, personal observation) and there is even a report of giant horsetails growing near sea level along streams in western Ecuador (Haught, 1944). Hauke (1969b) described several cases wherein giant horsetail colonies in Costa Rica had disappeared, presumably due to the process of succession at once-suitable sites. Dr. Benjamin Ollgaard (2000, personal communication) has observed that giant horsetails are frequent pioneers on land and mud slides in the valleys of the Rio Pilaton and Rio Pastaza in Ecuador. Ollgaard suspects that these pioneer stands can probably persist until sufficient forest regeneration occurs to shade out the horsetails (after ~25-50 years).
The giant horsetails, like other Equisetum species, develop extensive underground rhizome systems. Unfortunately, there has been no study of the rhizome architecture of the giant horsetails. However, it is known that the rhizomes of E. telmateia (the largest member of the subgenus Equisetum) can extend more than 4 m deep into wet clay soil (Page, 1997). Anthony Huxley reported in the book "Plant and Planet" (1975, p. 243) that "field bindweed is recorded at a depth of 7 m and horsetails in light soil two or three times as deep again". This report suggests that Equisetum rhizomes may penetrate to the extraordinary depth of 21 m in certain situations! Unfortunately, Huxley did not mention his source for this report or the species and location involved, so it would be proper to remain skeptical of this claim.
Rhizome segments that are exposed by erosion and broken-off can be carried downstream to establish new clones (Hauke, 1969b). Equisetum species generally invest a large proportion of resources in rhizome growth. Borg (1971) found that E. palustre may produce more than 100 times more rhizome biomass than aerial stem biomass. Equisetum arvense also allocates the larger proportion of its dry matter to rhizomes and tubers, thought not to such an extreme extent as E. palustre (Marshall, 1986). The large pool of resources stored in Equsietum rhizomes facilitates aerial shoot regeneration if a distrubance destroys the aboveground stems. Hence, this growth strategy is adaptive for the types of disturbance-prone habitats favored by many equiseta, including giant equiseta. There have been no studies of the ratio of aboveground to belowground biomass allocation in giant horsetails. It would also be interesting to know whether the two subgenera of the genus Equisetum differ overall in their biomass allocation patterns.
The distribution and ecology of the giant Equisetum species of the American tropics, E. giganteum, E. myriochaetum and E. x schaffneri provide a striking example the importance of vegetative persistence of hybrids in the genus. These three species are largely confined to upper elevations between 150 and 3000 m. Equisetum giganteum is a giant species which grows up to 5 m in height. It is the most widespread horsetail in Latin America, ranging from Guatemala to Brazil, Argentina and Chile as well as on Hispaniola, Jamaica and Cuba (Hauke, 1963; 1969b). Equisetum myriochaetum is also a giant species and is known to grow to 8 m in height. Equisetum myriochaetum bas a more limited range and is distributed from southern Mexico to Peru (Hauke, 1963). There is also a widespread hybrid, E. x schaffneri, between these two giant horsetails which ranges from Mexico to Peru (Hauke, 1963). Although E. x schaffneri is sterile, it persists via vegetative reproduction and may form large colonies (Hauke, 1967). This hybrid is found throughout the region of overlap between its parent species, but it is also found in Mexico, where E. giganteum is not known to occur, and in Venezuela, where E. myriochaetum is not known to occur. This unexpectedly extensive distribution may be due to vegetative dispersal or to the production of an occasional, rare, viable spore (Hauke, 1963). Viable spores have been observed for other Equisetum subgenus Hippochaete hybrids (Krahulec et al., 1996), so this hypothesis appears plausible. Equisetum x schaffneri demonstrates the remarkable frequency and persistence of Equisetum hybrids.
Equisetum is a surprising case of an ancient and morphologically conservative plant genus, with many unusual characteristics and adaptations, that bas persevered across geological time and geographical and ecological space. These observations make a strong case for considering Equisetum "the most successful living genus of vascular plants" (Stanich et al., 2009; Rothwell, 1996; Bierhorst, 1971).
Acknowledgments I would like to thank the late Dr. Warren H. Wagner, Jr. for his encouragement to pursue studies of Equisetum. I also thank Dr. Jack Fisher for suggesting the development of this manuscript.
Published online: 15 January 2013
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Chad Husby (1,2)
(1) The Montgomery Botanical Center, 11901 Old Cutler Road, Coral Gables, FL 33156, USA
(2) Author for Correspondence; e-mail: email@example.com
Table 1 Morphological characters distinguishing giant Equisetum species. Compiled from Dr. Richard L. Hauke's (1963) monograph of Equisetum subgenus Hippochaete, unless otherwise referenced. Dr. Hauke's work was based upon intensive study and analysis of a large number of herbarium specimens. E. giganteum E. myriochaetum E. x schaj1heri Type Jamaica (or Vera Cruz, Mexico Orizaba, Mexico locality Hispaniola (a)) Distribution Cuba, Jamaica, Mexico, Central Mexico (c), (b) Hispaniola, America, Central America, Central American Colombia, Colombia, (Guatemala, El Ecuador, and Peru Venezuela (c), Salvador, Ecuador, Peru Honduras, Nicaragua (Luis Diego Gomez, 1985), Cost Rica, Panama), and South America (Venezuela, Colombia, Ecuador, Peru, Bolivia, Brazil, Paraguay, Uruguay, Chile, and Argentina) Habitat "... along rivers "In swampy places "... in springy, or in swampy or along rivers marshy places, or places, usually and streams, along rivers and shaded" usually at the streams." edge of or within forested areas ..." Altitudinal 150-2600 m 200-3000 m 500-3000 m range Maximum stem 5 m 8 m 4.5 m height (4) Maximum stem 2.4 cm (3.9 cm 1.8 cm 2.2 cm diameter (d) stem measured by Husby, unpublished data) Branch ridge "... square or "sawtooth pattern "... sawtooth to pattern flattened in oriented irregular." profile, in apically" Brazil, Peru, and southern South America tending to be irregular." Main stem "... in bands of "Stomata in one "... in bands of stomatal 3-4 (rarely 2-3 line on each side 1-2 (occasionally pattern or 4-5)" of the groove." 2-3)" Endodermal "Cross section "... double individual arrangement with separate common ..." endodermises endodermis around each vascular bundle (individual endodermises)" Sheath teeth "mostly "... usually thin "... mostly persistence persistent" and brown to smoothly shed." (Tryon & Tryon, white, drying and 1982) breaking off to produce a clipped appearance at the top of the sheath, or (especially in South America), the bases or much of the teeth persisting" Cones have a "short "blunt, or the "acute or with (about 0.5 mm) branch cones slight apiculum" but distinct frequently with a apiculum" slight apiculum" Sheath non-living, dry, living, green, living, green (C. condition at brown or gray in sometimes with E. Husby, stem color (C. E. black or brown personal maturity E Husby, personal pigmentation (C. observation) observation) E. Husby, personal observation) (a) Proctor (1985) and Lellinger (1989) gave the type locality as "presumably ... Hispaniola", whereas Hauke (1963) gave the locality as Jamaica (b) Only two other Equisetum species reach the tropics in Latin America, E. hyemale (which reaches Guatemala) and E. bogotense (From Costa Rica to Chile and Argentina) (Moran and Riba, 1995; Stolze, 1983) (c) Interestingly, this hybrid is found in Mexico, where its parent, E. giganteum, is not known to be present, and in Venezuela, where its other parent E. myriochaetum is not known to be present. Hauke (1963) hypothesized that this unexpected phenomenon may be due to occasional viable spores being produced by E. x schaffneri and the resulting plants persisting vegetatively. Viable spores have been observed for other Equisetum subg. Hippochaete hybrids (Krahulec et al., 1996), so this hypothesis appears plausible. Tryon and Tryon (1982) have suggested that E. x schaffneri may not be a hybrid at all, but rather an intermediate form of a single polymorphic horsetail species E. giganteum (with the currently recognized E. giganteum and E. myriochaetum representing extremes of this species). However, Hauke (1963) notes in support of E. x schaffneri's hybrid status that its spores are not viable in contrast to those of the other two species. The status of E. x schaffneri could probably be settled by attempting to synthesize E. x schaffneri from a cross of E. giganteum and E. in myriochaetum in the laboratory, as has been done for other subgenus Hippochaete hybrids (Duckett, 1979). Molecular taxonomic analysis would likely shed additional light on this question (d) These numbers are based on collectors notes and measurements of herbarium specimens
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|Publication:||The Botanical Review|
|Date:||Jun 1, 2013|
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