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Australian Journal of Botany, 2008, 56, 144–152

Aestivation organ structure in Drosera subgen. Ergaleium (Droseraceae): corms or tubers; roots or shoots? John G. Conran Centre for Evolutionary Biology and Biodiversity Environmental Biology, Discipline of Ecology & Evolutionary Biology, DP 312 School of Earth and Environmental Sciences, The University of Adelaide, SA 5005, Australia. Email: [email protected]

Abstract. The nature of the subterranean aestivation organ in Drosera subgen. Ergaleium is reinvestigated and expanded across a wider range of taxa. The structure is confirmed to be anatomically and developmentally a stem tuber, and the adventitious growths arising along the subterranean stem are confirmed as roots. The enveloping, multi-layered, tunicate, corm-like sheath seen in some species is of epidermal and not of leaf origin, so that the structure is a tuberous condensed rhizome and not a corm. Nevertheless, the resulting structures appear to function ecologically as corms, the sheaths possibly protecting the dormant tubers from dehydration, and/or the abundant droserone pigment in the sheath tissues acting to deter fungi and other organisms. Similarly, the adventitious root-like structures on the stems are found to be anatomically roots, albeit lacking a developed root cap, and to possess well developed, epidermally derived root hairs, contrary to the suggestion of some studies that the ‘hairs’ were ectomycorrhizal hyphae. However, many Ergaleium species have no sheaths, or use remnant stem and/or root tissues, and some other species appear to show sheath-related hyphal associations, and highly reduced roots with few or no obvious root hairs. Thus, the ecological strategies involving these structures remain an area for further study.

Introduction The members of Drosera subgen. Ergaleium (Droseraceae) are characterised in part by the presence in nearly all species of a subterranean stem-derived fleshy aestivation organ (Marchant et al. 1982; Schlauer 1996). The only exception is the fibrousrooted tropical Drosera subtilis N. G. Marchant, whose position in Ergaleium requires re-examination. This feature also appears to be a synapomorphy for the subgenus, and its basal position to the subgeneric clade is supported by a range of molecular and morphological features (e.g. Rivadavia et al. 2003; Conran et al. 2007). These dormancy organs fall into the following two types: paired, where the new season’s structure forms beside its parent; and internal replacement, where the new structure forms inside its parent. There have been several studies into the structure (Morrison 1905, 1907; Vickery 1933), ecology (Jeffrey 1967; Dixon and Pate 1978), physiology (Chandler and Andersson 1976; Pate and Dixon 1978, 1981, 1982; Dixon et al. 1980), phytochemistry (Russell 1959) and relationship to roots of structures associated with these aestivation organs (Diels 1906a; Goebel 1923). These studies, as well as more general texts covering the family (e.g. Lloyd 1942; Erickson 1968; Lowrie 1987; Juniper et al. 1989; Gregory 1998) have nearly all regarded these aestivaculae as being tubers. Curiously, although DeBuhr (1977) studied the above- and below-ground stem anatomy of 24 species in subgen. Ergaleium, he did not report their aestivaculum structure. Planchon (1848) and Morrison (1905, 1907), interpreted the multi-layered sheaths surrounding the fleshy dormancy organs to be analogous to a bulb, whereas Jeffrey (1967) and Schlauer CSIRO 2008

(1996, 2006) considered the aestivaculae to be corms. Schlauer (2006) stated ‘as the storage and resting organs in subgenus Ergaleium are covered by a leaf-derived, readily detachable envelope, they must not be called tubers (in which the adnate skin is not derived from leaves and detachable only but force or after cooking) but are instead what the botanist technically calls corms, cf. the analogous situation in Crocus or Gladiolus’. Most recently, Venugopal and Raseshowri Devi (2007) suggested that the sheaths were mycorrhizal in origin, at least for D. peltata Thunb. in India, resulting in part from hyphal invasion of the outer cortical layers of the aestivaculum by dark-septate ectomycorrhizal (DSE) fungi, although Droseraceae are generally considered to be non-mycorrhizal (MacDougal 1899; Peyronel 1932; Juniper et al. 1989), with only two earlier records; Schlicht (1888) for D. anglica Huds. (as D. longifolia L.) and D. intermedia Hayne (Fuchs and Haselwandter 2004). Accordingly, because there is ongoing contention as to the precise nature of these fleshy dormancy structures and their associated sheaths and root-like organs, the present study re-examines the previous anatomical and morphological investigations of aestivaculae and their associated structures in subgen. Ergaleium, incorporating additional material in order to help clarify the nature of these structures. Materials and methods Actively growing plants with attached aestivaculae (and lateral or epiphyllous stolons, where appropriate) were collected in late winter or early spring (the time new aestivaculae are formed) from wild-growing plants of D. auriculata Backh. ex Planch., 10.1071/BT07140

0067-1924/08/020144

Aestivation organ structure in Drosera subgen. Ergaleium

D. macrantha Endl. subsp. planchonii (Planch.) N.G. Marchant, D. peltata, D. praefolia Tepper, D. stricticaulis O.H.Sarg., D. whittakeri Planch. subsp. whittakeri, subsp. aberrans Lowrie ex Lowrie & Carlquist, and the ‘Kangaroo Island’ form of D. whittakeri mentioned by Clayton (2003). Nomenclature follows CHAH (2006). Morphological characteristics were photographed on live plants, and tissues were then fixed in formaldehyde–70% ethanol–glacial acetic acid (10 : 85 : 5) for at least 24 h and stored in 70% ethanol. After standard paraffin wax embedding (Johansen 1940), they were sectioned longitudinally at 10–15 mm and the slides stained successively in 1% aqueous acid fuchsin and 0.5% aqueous toluidine blue O (O’Brien and McCulley 1981), destained in distilled water, dehydrated and mounted in Gurr’s DePeX (BDH Chemicals, Poole, Dorset, UK). The slides were examined microscopically, organs and tissues identified and the results compared against previous anatomical work. In addition to the sections stained with toluidine blue O, tissues for mycorrhizal investigation were also prepared following the methods of Vierheilig et al. (1998, 2005). Samples were boiled for 3–5 min in 10% w/v KOH until cleared, rinsed with tap water for 5 min, then boiled for 3 min in a 5% solution of Sheaffer jet black Skrip ink (Sheaffer Eaton (Textron), Fort Madison, IO, USA) diluted with domestic vinegar (~5% acetic acid). The tissues were then destained for 20 min in tap water acidulated with a few drops of vinegar, mounted in Crystalmount (Fisher Scientific, Pittsburgh, PA, USA) and photographed under light microscopy. Results Morphology In dormant aestivaculae, the new season’s bud is adjacent to the attachment scar of the now dead shoot from which the aestivaculum developed during the previous season (Fig. 1A). In actively growing plants, scale leaves occur along the underground portion of the primary, vertical shoot (the stolon sensu Marchant et al. (1982) and Lowrie (1987)) and the lateral shoot/stolon that generates the replacement dormancy organ (Fig. 1B, F). There are also reduced root-like structures which develop in the axils of the scale leaves or at their bases (Fig. 1B, D–H). The shoot that bears the replacement dormancy organ normally arises in the axil of a scale leaf just above the parent (Fig. 1E, G–I), but often penetrates more deeply into the soil (Fig. 1E, see also Dixon and Pate 1978; Pate and Dixon 1982). Secondary, daughter aestivaculae can also form in scale-leaf axils, particularly if the parent is damaged or removed (Fig. 1F). In contrast, proliferating lateral shoots (Fig. 1B) generally arise at, or above, ground level from either scale, or fully developed leaves remote from the aestivaculum. Because both the replacement and daughter aestivaculae commonly develop on positively geotropic axillary shoots, the shoots that bear them are called ‘droppers’ (Vickery 1933; Dixon and Pate 1978). The apex of this replacement and/or proliferation shoot initially grows downwards (Fig. 1B) but then inverts, becoming anatropous (Figs 1C, 2A; also Vickery 1933) and swelling to create the replacement structure (the ‘probulb’ of Morrison 1905). In ‘paired organ’ species, if the parent is at an optimal depth, its replacement tends to grow beside it (Fig. 1D–E, G), expanding to

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fill the space left as the parent withers (Figs 1G, 2A; see also Vickery 1933). In species with internal replacement, such as D. erythrorhiza Lindl. and its close relatives, the shoot/dropper grows back down into the parent organ (Fig. 1H, see also Russell 1959), developing inside the degenerating parent tissues (Figs 1H, I, 2B, D). A common feature in both paired and internal species is the production of a bright red free pigment (droserone), either from the degenerating parent (Fig. 1B, H, I) and/or developing directly in the epidermal tissues of the replacement organ (Fig. 1H–I). Many species also develop fibrous shoot channels derived from the remnants of previous season’s vertical shoots (Fig. 1B); some species even without sheaths around the dormancy organ (e.g. D. macrantha subsp. planchonii) still develop channels (Fig. 1E). Anatomy As the parent organ is depleted, the epidermis and outer layers of the cortex parenchyma detach from the inner cortex and vascular regions (Fig. 2A, C). The remnant parent epidermis thus creates a dark, apparently two-layered, concave shell on one side of the replacement tuber (Fig. 2A, C; see also Vickery 1933). Replacements tend to alternate sides with the parent in successive years, so that in time previous epidermal shells end up fully enclosing the paired organs (Fig. 2A). In ‘paired organ’ species, these inner tissues further reduce by autolysis, shrinking in tandem with expansion of the adjacent new season’s organ (Fig. 2A). Species with internal replacement have the remnant skins of previous season’s tubers already surrounding the replacement from its earliest development (Fig. 2B, D; also Russell 1959; Dixon and Pate 1978), but in this instance, the sheath is single-layered as it lacks the ‘second’ layer caused by the laterally compressed epidermis of an adjacent tuber (Fig. 1D). In some species, there is also further enclosure of the aestivaculum by fibrous root and/or shoot remnants (Pate and Dixon 1982; Lowrie 1987) and/or associated fungal hyphae (Fig. 2E, F; also Venugopal and Raseshowri Devi 2007). Growing out from along the lower dropper stems (Fig. 1B–D, G), as well as in and around the outside of the sheath layers (Fig. 2A, C), were numerous short stem-derived roots. Although generally smooth or slightly papillate, the roots in some species, such as D. whittakeri, were densely covered with long root hairs (Fig. 3A, B). In transverse section these roots were often small and/or relatively reduced (Fig. 3C), as was also noted by Venugopal and Raseshowri Devi (2007); however, anatomically they still showed a well developed epidermis with root hairs, and a 2–4-layered cortex of thin-walled parenchyma. A pericycle was obvious but not strongly thickened, and the central vascular tissue of the stele showed weak organisation and generally little obvious wall thickening or clear differentiation between the proto- and metaxylem. Although none of the roots examined in the present study showed clear mycorrhizal associations, in some cases the degenerating tissues associated with the sheath layers from previous tubers were associated with branching, fungal hyphae of the DSE type described by Jumpponen and Trappe (1998), Jumpponen (2001) and Fuchs and Haselwandter (2004) (Fig. 3D). These DSE hyphae were found within the sheathing

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remnants of previous epidermal layers, but were not the primary tissue seen in these structures. There was no evidence of any mycorrhizal zone or Hartig net development within live aestivaculae in any of the species examined, neither for degenerating or developing replacement tissues, nor were they found in the roots.

Discussion Aestivaculae Vickery (1933) and Russell (1959) described the morphological and anatomical changes that occur during aestivaculum generation in D. auriculata, D. gigantea Lindl., D. peltata (all

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paired species) and D. erythrorhiza Lindl. (an internally replaced species), but did not illustrate anatomy. My results for the additional taxa and morphotypes studied here were consistent with their findings, as well as with some of the aestivacular anatomy illustrated in Venugopal and Raseshowri Devi (2007). Part of the problem in defining the dormancy structure in subgen. Ergaleium comes from the varied and often nonexclusive or overlapping botanical definitions for tubers and corms, as both are fleshy forms of modified, compressed rhizomatous stems or buds (e.g. Bell 1991; Judd et al. 2002; Raven et al. 2005; Rost et al. 2006). Harris and Woolf Harris (2001) defined a corm as ‘a short, solid, vertical underground stem with thin papery leaves’ and a tuber as ‘the thickened portion of a rhizome bearing nodes and buds; underground stem modified for food storage’. Benson (1979) similarly distinguished a tuber as ‘the thickened portion of a rhizome is a tuber. The best known example is the white potato; this species produces slender underground branches forming thickened tubers at their ends. Like other stems the tuber is covered with buds, which develop in the centers of the eyes of the potato. Thickened root are not tubers’. In contrast, he defined a corm as ‘Some stem [sic] (e.g. those of Brodiaea and Crocus) form bulblike structures underground. These tuberous enlargements of the stem are called corms or solid bulbs. Many corms are covered with thin membranous coats’. Hickey and King (2000) showed a corm developing vertically, with the replacement corm developing apically on its parent and the adventitious roots developing directly from the parent corm’s base; the whole structure enveloped in a series of large scale-like leaves or leaf bases. However, their tuber has axillary buds from which new roots arise adventitiously, reduced scale leaves, and daughter tubers arising from axillary lateral shoots or stolons. Among the most detailed definitions of the different types of subterranean vegetative storage organs are those of Pate and Dixon (1982), and the modified version of their classification in Menkins (2002). Their definitions for corms and for paired, stemderived tubers can be summarised as follows: Corms: swollen, compacted, vertically oriented subterranean stems with well defined apical meristems, and previous shoot, inflorescence and root positions indicated by scar tissue. Corms have the main storage tissues within the corm itself, but remnant leaf bases from previous seasons may form a protective sheath. Adventitious roots may arise basally and laterally on previous or current nodal tissue. Unlike bulbs, corms develop inflorescences only after the current season’s growth has commenced. New tissues are produced on top of, or beside old ones, which may create a jointed structure. Corms


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may reproduce by lateral offsets arising from superficial buds on the parent corm, or by primary shoot apex division before the replacement corm matures. Stem tubers: any regular or defined swelling of a fleshy underground stem. Paired stem tubers arise on modified underground shoots from swollen, modified lateral shoots arising separately on an otherwise normal shoot system. The pair occurs vertically, often side by side, and originates from the axil scale leaves at a basal stem node. The parent tuber represents the previous season’s growth; the replacement tuber, the current season. There is a range of dormancy and storage organs within Droseraceae, with protective leaf-derived sheathing structures covering the dormant buds of Dionaea muscipula Ellis (corms) and Aldrovanda vesiculosa L. (scale-covered, cormous? turions) (Rea et al. 1983; Adamec 2003). Similarly, the stipule- and petiole-derived aestivaculae of Drosera subgen. Bryastrum and sect. Lasciocephala, and the leaf-base derived hibernaulae seen in some species of subgen. Drosera and Arcturia (Slack 2000), more or less fall between the functional definition of a corm and a bulb, depending on the volume and compression of the dormant tissues encased, and the degree of fleshiness of the ensheathing leaf-derived structures. Similarly, the root-derived thickened, fleshy storage/ dormancy organs of Drosera sect. Ptycnostigma (Diels 1906b) qualify as root tuberoids, whereas the thick, but non-tuberous roots of D. binata Labill. (subgen. Phycopsis) and D. hamiltonii C.R.P.Andrews (subgen. Stelogyne) are also used for summer dormancy and post-fire regeneration. This shows that in both Droseraceae and in other geophytes from similar habitats, the development of functionally and morphologically similar fleshy storage and dormancy organs can arise in several ways. One feature that makes the dormancy organs of Ergaleium appear corm-like is their vertical orientation and apparently single dormant bud. However, the replacement and secondary (dropper) corms in stoloniferous, corm-bearing taxa such as Brodiaea (Themidaceae) the new corm shows orthotropous development, whereas the apical shoot inversion in Ergaleium spp. means they are anatropous. In addition, whereas lateral corm development is normally ‘fixed’ (i.e. once the shoot forms, only a corm will result), Ergaleium spp. often show deviation of the dropper apex into ‘normal’ leafy rosettes or shoots after prolonged exposure to light (Vickery 1933; Dixon and Pate 1978; Pate and Dixon 1981, 1982). Furthermore, if the shoot is removed early from the parent organ, resprouting occurs from axillary buds in the scale leaves at the aestivaculum apex.

Fig. 1. Aestivaculum morphology of sheathed and non-sheathed members of Drosera subgen. Ergaleium. (A) D. stricticaulis dormant tuber; black arrow indicates a scar from previous season’s shoot; white arrow indicates new season’s dormant bud. (B) D. whittakeri subsp. aberrans; black arrow indicates degenerating parent tuber producing droserone as free pigment; white arrow indicates lateral dropper with scale leaves. (C) D. auriculata with droserone-rich dropper apex inverting to form replacement tuber. (D) D. auriculata; black arrow indicates parent tuber and sheathing remnant of an earlier season’s tuber skin; white arrow indicates replacement tuber. (E) D. macrantha subsp. planchonii with unsheathed replacement tubers and showing fibre channel enclosing the new season’s shoot. (F) D. whittakeri ‘Kangaroo Island form’ shoot some weeks after tuber removal; black arrow indicates ‘new’ replacement tuber from a basal leaf scale; white arrow indicates daughter tubers from lower stem scale leaves. (G) D. auriculata tuber in section; black arrow indicates parent degenerating tuber and detached skin; white arrow indicates replacement tuber. (H) D. whittakeri subsp. aberrans tuber in section; black arrow indicates an attachment scar of parent tuber to shoot; white arrow indicates droserone granules inside internal replacement tuber. (I) D. whittakeri subsp. aberrans tuber in section; black arrow indicates bud of

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Fig. 2. Aestivaculum anatomy in Drosera subgen. Ergaleium. (A, C) D. auriculata; (B, D) D. whittakeri subsp. aberrans. (A) Longitudinal section through paired aestivaculum complex, showing degenerating (DA) and replacement (RA) structures, epidermally derived sheaths from previous seasons (ES), extant epidermal tissues (Ep), specialised reduced roots (RR), and developing new season’s shoot apex with meristem (Me) and scale leaves (SL). (B) Longitudinal section of an internal replacement aestivaculum (labelled as per A). (C) Close up of degenerating aestivaculum, reduced specialised root and tunicate sheath, showing two-layered appearance of the latter owing to lateral compression of the epidermis following internal tissue degeneration (labelled as per A). (D) Close up

Development is apparently also triggered by heat and/or water stress causing the release of aestivaculum-forming cytokinins (Darnowski et al. 2003).

In the majority of Drosera subgen. Ergaleium, the aestivaculae replace the previous season’s organ and do not, or only very rarely, generate daughter plants (Vickery 1933; Dixon



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Fig. 3. Adventitious root anatomy and possible fungal associations in Drosera subgen. Ergaleium. (A, B) D. whittakeri subsp. whittakeri; (C, D) D. auriculata. Cleared whole mount of root, (A) showing dense root-hair development, and (B) epidermal root-hair origin and absence of mycorrhizal development. (C) Transverse section through root growing through sheath tissues, showing degenerating, epidermally derived sheaths from previous seasons (ES), root epidermis (RE), root hairs (RH), parenchymatous cortex (Co), thickened pericycle (Pe) and weakly thickened, poorly organised stele (St). (D) Transverse section of previous seasons’ aestivacular sheathes, showing dark septate fungal hyphae (Hy) development in the remnant sheath tissues (ES). Scale bars = 100 mm. Vouchers, A, B: JGC 2008; C, D: JGC 2011 (all ADU, AD).

and Pate 1978); however, there are a small number of taxa where propagation occurs through the development of lateral, aestivaculum-forming shoots (referred to as roots in Adlassnig et al. 2005). This can occur by subterranean laterals in D. erythrorhiza subsp. erythrorhiza (less commonly in the other subspecies), D. macrophylla Lindl., D. marchantii DeBuhr subsp. marchantii and D. zonaria Planch. It can also occur through stolons (D. macrantha subsp. eremaea N.G. Marchant & Lowrie; Drosera monticola (Lowrie & N.G. Marchant) Lowrie and D. whittakeri subsp. aberrans). Less commonly, some members of sect. Ergaleium propagate by descending axillary shoots from aerial epiphyllous buds, as happens rarely in D. auriculata and D. peltata (Vickery 1933), and abundantly in a recently discovered form of D. moorei (Diels) Lowrie (A. Lowrie, pers. comm.).

Planchon (1848) and Morrison (1905) considered that the shells forming the tunic around the aestivaculum were leafderived and therefore that the dormancy organs were bulbs. Jeffrey (1967) and Schlauer (1996, 2006), although recognising that the dormancy organs were not bulbs, still considered the sheaths to be leaf-derived, regarding the aestivaculae as corms. Anatomically to be a corm, the sheathing layers should be of leaf origin, whereas in a tuber, the outer surface is of stem origin and epidermal. Accordingly, as the sheaths in Drosera subgen. Ergaleium are epidermal remnants from previous seasons, the dormancy organs are anatomically tubers. Ecologically, the structures appear to function in the same protective manner as the leaf-derived tunic of a corm, but here the condition has arisen convergently and the sheaths are not

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homologous. The sheaths in many Ergaleium species show longterm resistance to breakdown, leading to multi-layering, and in some cases up to 60 layers may result, indicating extreme longevity (Lowrie 1987). It is assumed that the sheaths afford desiccation resistance during dormancy (Vickery 1933; Russell 1959; Dixon and Pate 1978). In addition to the sheaths, some species also develop a ‘shoot channel’ from the subterranean remnants of the vertical stems from previous seasons (Vickery 1933; Russell 1959; Lowrie 1987). This channel may be fibrous (many species), papery (e.g. D. fimbriata DeBuhr and D. platypoda Turcz.), and/or include fibrous, root-derived tissues (Russell 1959; Lowrie 1987). There are even fibrous channels in D. macrantha subsp. planchonii and D. gigantea, despite the absence of epidermal tuber sheaths in these species. The channel is thought to help protect emerging new season’s shoots pushing through the soil (Vickery 1933), and a similar function was postulated for the mucilaginous exudate that covers the otherwise unprotected shoots of D. stolonifera Endl. s.str. (Lowrie 1987). The fibrous shoot channel was also thought to act as a velamen-like conduit for moisture passage to, and retention around, the tuber (Rendle 1925). Possibly because of this, these channels are also locations for small secondary tubers which form on short axillary droppers in and along the vertical stems of D. platypoda and D. gigantea (Lowrie 1987). Nevertheless, there are numerous tuberous Drosera species which have no enclosing sheaths and/or shoot channels (Pate and Dixon 1982; Lowrie 1987), many of which also grow in the same habitats and conditions as the tunicate- and shoot channel-possessing species. The nature of any alternative anatomical adaptations needs to be investigated for these taxa. The adaptive value of these presumed desiccation protection structures also needs to be assessed carefully in light of long-term relative survival rates and/or physiological adaptations between the different co-occurring morphological tuber forms. The internal replacement strategy seems to occur in all members of sect. Erythrorhiza so far examined (Pate and Dixon 1982), whereas unsheathed tubers are found only in the D. macrantha–D. stricticaulis (Diels) O.H.Sarg.–D. pallida Lindl. complex and the D. gigantea complex (Lowrie 1987, 1998), both of sect. Ergaleium, suggesting a phylogenetically derived phenomenon. The implications of these different strategies need to be assessed to see if there are evolutionary, ancestry-related factors involved, or if they represent convergent adaptations. Roots Droseraceae generally have weak root systems (Adlassnig et al. 2005), although they are generally more extensive in stilt-rooted pygmy Drosera spp. (subgen. Bryastrum) where they are involved in temperature regulation (Pate et al. 1984), rootpropagating taxa such as D. hamiltonii (unpubl. obs.) and in some tuberous Drosera spp. from nutrient-poor dryland soils, where they are important for potassium uptake (Dixon and Pate 1978; Pate and Dixon 1982). The root-like structures arising along the stems in Drosera subgen. Ergaleium have been interpreted variously as roots (Vickery 1933; Russell 1959), specialised, possibly reduced roots (Adlassnig et al. 2005),

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zweifelhafte Wurzeln (dubious roots) (Goebel 1923), lateral organs of foliar origin (Venugopal and Raseshowri Devi 2007) or Blattrhizoiden (leaf-rhizoids) (Diels 1906b). They are anatomically similar to roots on the basis of the position of the meristem and starch grains and the presence of hair-like outgrowths (Diels 1906b), but they lack a root cap and (in many species) clearly defined root hairs, and as such do not fit the criteria for roots outlined by Goebel (1898, 1923). Nevertheless, in the present study, unlike the very heavily hyphae-infected images shown in Venugopal and Raseshowri Devi (2007), these root-like structures showed development of an epidermis, cortex, pericycle and stele, suggesting that at least some of them are anatomically close to being roots. Furthermore, in some species, there is considerable root-hair development in the root-like structures, making them roots in all things except a root cap. Goebel (1898) also noted that there were numerous exceptions to plants lacking root caps and yet still possessing what he regarded as ‘true’ roots; therefore, these adventitious structures arising from the subterranean parts of the stems in subgen. Ergaleium would seem to be true roots, albeit with various levels of reduction on some species. Many tuberous Drosera spp. also produce large quantities of droserone, a red, free pigment, throughout their tissues and around their tubers (Russell 1958, 1959; Juniper et al. 1989). This pigment is a water-soluble naphthoquinone which is widespread in Droseraceae, especially the in the tuberous taxa, and known to have antibacterial and possibly allelopathic and anti-feedant properties (Juniper et al. 1989). Russell (1959) suggested that the large mass of free droserone in internally replaced species was produced by autolysis and oxidation of the parent tuber, resulting in granules, crystals and an amorphous, damp, paste-like plug at the interface between the replacement and parent tuber. It is possible that the pigment deposits confer protection not only to current tubers, but also by slowing the breakdown of previous season’s sheaths by bacteria and soil fungi, adding to summer desiccation resistance. Nevertheless, D. praefolia lacks obvious free pigment in the tubers (Bates 1991), but produces just as many breakdown resistant sheaths as the droserone-rich D. whittakeri with which it grows. Accordingly, as with the tunics, the function of the pigment deposits requires further ecological and physiological investigation, and is currently the subject of ongoing research. Mycorrhizae Despite the presence of droserone in many Ergaleium spp. (and other Drosera spp.), the tunicate sheaths and outer tuber cortex in at least some taxa are associated with fungal hyphae, as are the roots of at least one species (Venugopal and Raseshowri Devi 2007), suggesting that if droserone acts as a fungicide, it does so selectively, and/or the fungi are immune to its effects. However, despite the presence of hyphae in some sheaths, the fungal mantle hypothesis for their origin proposed by Venugopal and Raseshowri Devi (2007) was not supported, since most of the taxa examined here lacked associated hyphae. Even in those taxa that possessed them, the sheaths were derived from Drosera epidermal and degenerate aestivaculum contents, with fungal association a secondary feature and possibly just evidence of opportunistic saprophytism.


The finding that the ectomycorrhizal DSE symbiont on D. peltata in India was probably the bolete fungus Suillus luteus (L. : Fr.) Roussel is interesting, given that neither this fungus, nor its mycorrhizally associated host tree genus Pinus L., is native to Australia. Added to this, the fact that most DSE fungi so far examined seem to be Pezizales rather than Boletales (Jumpponen and Trappe 1998) indicates that the DSE fungi growing with the Australian species of Drosera subgen. Ergaleium require investigations to see which fungal agents are involved and how they interact with their hosts. This is a subject of ongoing study. The dormancy organs in Drosera subgen. Ergaleium seem to follow a trend in southern Australian geophytes of behaving ecologically like corms (Parsons 2000; Parsons and Hopper 2003). Nevertheless, this convergent pattern is seen in both the stem-derived tunicate tuber sheaths in Drosera, and the structurally similar root-derived tuberoid sheaths in some native Orchidaceae, as well as the numerous native geophytes with true corms. The interesting question then arises as to why are there so many cormous plants in Australia relative to other geophyte-rich areas with equivalent climates but where bulbs dominate? Even more interestingly, why are some Australian geophytes modifying tubers or tuberoids apparently to function ecologically as corms? Tuberous roots and corms are generally much more common in southern Australia than are bulbs, stem tubers or rhizomes across all vascular plants, contrasting with other parts of the world with Mediterranean climates and abundant geophytes (Parsons 2000; Parsons and Hopper 2003). Unfortunately the reasons for this are unclear, although phylogeography has been suggested as a factor, with the morphology of the first species to arrive in an area influencing its descendants (Parsons and Hopper 2003). The subterranean resting and storage organs in many Australian native terrestrial Orchidaceae are also morphologically and ecologically very similar to those seen in Droseraceae, with which they often co-occur. This includes the development of droppers, parent, replacement and laterally displaced daughter structures. In Glossodia R.Br. and Cyanicula Hopper & A.P.Br., the parallel even extends to the development of an enclosing, multi-seasonal epidermal ‘sheath’ (J. Drummond, quoted in Lindley 1839; Hoffman and Brown 1992). Nevertheless, these almost identical fleshy organs, despite containing an apical bud from which the new shoot and adventitious roots ultimately arise, are of root origin and thus defined as tuberoids, rather than tubers (Jones 1988). It has been noted that protection of dormant organs from dehydration over the dry summer months is important (Pate and Dixon 1981, 1982) and certainly, the persistent, papery, often many-layered covering on the aestivaculae of many Drosera subgen. Ergaleium species resembles the condition seen in a tunicate corm, at least in a functional sense. The tunicate aestivaculae in Drosera subgen Ergaleium are developmentally and anatomically stem-derived, but appear to be tubers rather than corms. The multi-layered corm-like sheaths seen in some species are the persistent remnants of the epidermal layers of previous season’s tubers, and are again, neither leaf- nor mycorrhizally derived (although they can be fungally infected). Thus, although the aestivaculae may be functionally corm-like,


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possibly affording protection against desiccation, they are anatomically tubers and at best might be termed ‘pseudocorms’. However, as there are also numerous species in subgen. Ergaleium where either no sheaths develop, or where the protective structures also involve fibrous or papery remnant stem and/or root tissues, the use of potentially misleading terms such as ‘pseudo-cormous tuber’ is not advised. Acknowledgements The Discipline of Ecology & Evolutionary Biology, School of Earth and Environmental Sciences at The University of Adelaide, is thanked for the provision of resources to undertake this study, as is the Department of Anatomical Sciences for sectioning the samples. The South Australian Department of Environment and Heritage is thanked for permission to collect specimens from lands under its control. Professor Paula Rudall and Associate Professor Jose´ Facelli are thanked for comments on the manuscript.

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Manuscript received 24 July 2007, accepted 30 October 2007

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