Gunneraceae

Gunneraceae Meissner, Pl. Vasc. Gen., tab. diagn.: 345, 346; Comm.: 257 (1842), nom. cons.

H.P. Wilkinson and L. Wanntorp

Perennial herbs, either with ascending or creeping pachycaulous stems, covered with large leaf scars, apically with large to gigantic, long-petioled leaves reaching up to c. 5 m in height (G. magnica), and between these often covered with conspicuous bracts protecting the inorescence and vegetative buds, or stoloniferous and mat-forming, with short, upright stem portions bearing leaf-rosettes, reaching from 4 cm to about 1 m in height, or in one case (G. herteri), diminutive annuals. Leaves alternate, crowded at stem tips; petioles short to very long; lamina oblong to reniform or peltate, dentate, crenate or palmately lobed, the crenations and lobes with protruding hydathodes; venation in large-leaved species palinactinodromous with veins very prominent and projecting as ribs on abaxial surface, in smaller-leaved species actinodromous or pinnate and less prominent. Sometimes with more or less conspicuous, simple to much divided scales between the leaf-bases, stolons with paired, or single ochrea-like, bracts apically. Inorescences axillary or pseudoterminal, erect, simple or compound racemes, or spikes; lower owers mostly pistillate, upper ones staminate, the middle ones sometimes perfect, or owers all unisexual, in a few cases plants dioecious. Flowers small, bracteate or not, epigynous, sepals 2, anteri-posterior, valvate, sometimes obsolete, petals 2, transversal, mitre-shaped, slightly exceeding the sepals, caducous, in female owers wanting; stamens 2(1), transversal, with short laments; anthers dithecal and tetrasporangiate, opening by longitudinal slits; carpels 2, united to form an inferior, unilocular ovary; stylodia 2, transversal; stigmas dry, papillate; ovule solitary, pendulous from apex of locule. Fruit drupaceous, coriaceous to eshy, oval to globose, green or bright red, rarely white or yellow. Seeds with a very small obcordate embryo embedded in copious, oily endosperm. Specialized organs containing endosymbiontic Nostoc cells are located in the stem between the leaf-bases of all species.

A monogeneric family with about 60 species, growing in cool and wet or damp habitats, from low altitudes to above 3,000 m, in South and Central America, Mexico, Hawaii, Africa, Madagascar, Tasmania, New Zealand, New Guinea and the Malayan archipelago Vegetative Morphology. Gunnera comprises a wide spectrum of growth forms from giant to dwarf herbs, usually perennial, with erect or creeping stems, often forming mats or clumps by stolons originating from leaf axils on the stems and bearing leaf-rosettes apically, or more rarely by branching of the stems themselves (Figs. 59, 63). The main stem of the dwarf G. herteri is interpreted as a chain of sympodial units each consisting of a leaf and an extra-axillary inorescence (Rutishauser et al. 2004), a structural pattern which may also be valid for other species of Gunnera (see Skottsberg 1928). Stolons occur in subg. Pseudogunnera, Milligania and Misandra. In Pseudogunnera and Milligania, two bud scales at the tip of the stolons precede the foliage leaves on the erect stem. These cataphylls are regarded by Wanntorp et al. (2003) to be homologous with a cap-like ochrea, which in subg. Misandra occurs on the stolon as well as between the leaves of the upright stem. In subg. Panke, in which no stolons are formed, the stems are covered by numerous, large bract-like scales. Skottsberg (1928) and Wanntorp et al. (2003) consider also these scales to be cataphylls. Vegetative Anatomy. (Information mostly from Wilkinson 1998, 2000). Nodes are multilacunar and multitrace. Leaves are bifacial, hypostomatous or amphistomatous; stomata are anomocytic. The lower leaf surface has always a smooth wax cover; the cuticle is smooth or (in some species of subg. Milligania) nely striate. Marginal leaf hydathodes with an epithem are found in all subgenera (Fig. 59D), while laminar hydathodes are restricted to subg. Panke. The leaf axils of Gun-

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nera herteri contain 25 inconspicuous glandular colleters (Rutishauser et al. 2004). Unicellular hairs are widespread and lacking only in G. herteri; other hair types including uniseriate and multiseriate, stalked and globular hairs are found in subg. Panke. Domes of raised silicied cells (warts) on the upper leaf surface and spine-like emergences on petioles and the larger veins of the lower leaf surface are characteristic of subg. Panke (Fig. 59C, E). The vascular systems of stems and petioles are typically polystelic. The bundles have the xylem surrounded by about six portions of phloem (amphicribal) and are sheathed by a well-dened endodermis with Casparian thickenings. In the stems of the pachycaulous, non-stoloniferous subg. Panke, the bundles may amount to several hundred per stem and in subg. Gunnera to about 60. Among the stoloniferous subgenera, the large-leaved subg. Pseudogunnera and the small-leaved subg. Milligania and Misandra have only few (35) larger and some smaller bundles, the latter to leaves and inorescences. The vascular tissue of the stolons is not polystelic but siphonostelic (-modied); it consists of a single tube of xylem and phloem (G. densiora), or of tubes of internal and external phloem separated by two tubes of xylem, and is surrounded by an endodermis. Vessel elements are usually very to moderately small; perforation plates in stolons and roots are mainly scalariform with few to many bars, and in the stems of large-leaved species simple perforation plates are more common. Cluster crystals (druses) are widespread in various tissues. Behnke (1986) found sieve element plastids containing protein crystals and starch grains (Pcs type). Flower Structure. The oral symmetry of Gunnera is most remarkable: the petals, stamens and carpels at least the stylodia are located in the transverse plane (Wantrop and Ronse De Graene 2005), reminiscent of the position of these oral organs in Sabiaceae and, to some degree, in Proteaceae.

Embryology. In Gunnera macrophylla and G. chilensis, the pollen grains are two-celled at anthesis. The ovule is anatropous, bitegmic and crassinucellate, and the micropyle is formed by the inner integument alone. The embryo sac is tetrasporic and 16-nucleate (Peperomia-type) and, apart from the egg and the synergids, contains six antipodal cells and a group of cells fusing to form the secondary embryo sac nucleus. Endosperm development is cellular; the suspensor forms no haustorium (Modilewski 1908). Pollen Morphology. Pollen of Gunnera is very distinctive, tricolpate, suboblate spheroidal (Fig. 60), and can be recognised by the fossaperturate shape with bulging mesocolpia and the microreticulate exine, usually 2028 2537 m (Erdtman 1952; Praglowski 1970; Jarzen 1980; Wanntorp et al. 2004). Karyology. Beuzenberg and Hair (1963) reported 2n = 34 for Gunnera monoica, G. prorepens, G. densiora, G. dentata and G. hamiltonii, and several hybrids (all in subg. Milligania); the same number was counted for various South American species by Dawson (1983) and Pacheco et al. (1993) Pollination. Gunnera perpensa shows all attributes of wind pollination (the general condition in the genus), such as high pollen/ovule ratio, strong protandry in the hermaphroditic owers, and starch storage in pollen (Lowrey and Robinson 1988). Fruit and Seed. The fruit is drupaceous, greenish-reddish, dry and relatively small (12 mm long) in subg. Panke, Pseudogunnera and Gunnera, in subg. Misandra and Milligania larger (up to 8 mm long), and often brightly coloured; G. magellanica is called frutilla del diablo, devils strawberry. In the maturing seed, the integuments and nucellus disappear, with the exception of the outer epidermis of the outer integument which is made up of thin-walled cells lled with red sap; mechan-

Fig. 59. Gunneraceae. AC Gunnera manicata growing in the Royal Horticultural Societys garden at Wisley, Surrey, UK. A Whole plant. B One leaf measuring 94 in. (237.5 cm) in width and 77 in. (195.5 cm) in length. C An inorescence (in spring) c. 2 ft. tall; note petiole with spine-like emergences to the right. D Marginal hydathodes

with terminal glandular tubes from a very young leaf of G. chilensis, scale bar = 1 mm. E Warts on the adaxial surface of a mature leaf of G. chilensis, scale bar = 0.25 mm. F Nostoc heterocysts in two large cells from a stem of G. lobata, scale bar = 50 m. G Heterocysts from F at arrows, scale bar = 10 m. (Orig. H. Wilkinson)

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Fig. 61. Gunneraceae. Summary tree of Gunnera, based on Wanntorp et al. (2002, 2003).

Fig. 60. Gunneraceae, pollen grains. A, B, E, F Gunnera chilensis, SEM micrographs. C, D G. macrophylla, light micrographs. A Polar view. B, E Equatorial view. C, D Optical sections showing thickened exine at colpi margins (C) and poles (D). F Equatorial view of one colpus and reticulate ornamentation. AE 1,000; F 51,500. (A, B, E, F Photographs H. Wilkinson; C, D photographs M.M. Harley)

gene regions by Wanntorp et al. (2002), and Wanntorp and Wanntorp (2003) resolved Gunnera as monophyletic and conrmed the sectional classication proposed by Schindler (1905). Moreover, subg. Ostenigunnera with the diminutive G. herteri was recovered as sister to all remaining sections, with subg. Gunnera subsequently sister to the remaining subclades. Figure 61 represents this topology with an indication of gains and losses of several characters. Gunnera herteri lacks the polystelic condition characteristic of the rest of the genus (the bundles are not sheathed by an endodermis; Wilkinson 2000); it is unique in being an annual, and possibly in the concaulescence of vegetative branches and inorescences with the main axis for some distance above the axil. Afnities. Gunnera has traditionally been included in Haloragaceae but has often been elevated to family rank, although its afliation has remained uncertain; Takhtajan (1997) included it in his Saxifraganae. Numerous molecular studies have now recovered Gunneraceae in close association with Myrothamnaceae in a clade at the base of the eudicots, more precisely as sister to all remaining core eudicots (Soltis et al. 2000, 2003). A comparison of the characters of Gunnera and Myrothamnus (Wilkinson 2000) shows that there exists very little agreement morphologically between the two genera. Distribution and Habitats. Gunnera is mostly southern hemispheric in distribution, but in South and Central America, the Hawaiian islands and Malesia it extends into low northern latitudes.

ical protection of the seed is taken over by the pericarp. The endosperm is copious, its cells containing oil, starch and aleurone with crystalloids. The embryo is very small, heart-shaped and lies excentric (Netolitzky 1926). Phytochemistry. The leaves of Gunnera manicata contain high concentrations of an unidentied ellagitannin (Doyle and Scogin 1988); in G. chilensis, the tannin content of the rhizomes amounts to 9.3% (Hegnauer 1966). Pacheco et al. (1993) have studied the avonoid variation of various South American species Relationships Within the Family. Cladistic analyses of Gunnera based on nuclear and plastid

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The species prefer wet or damp, cool places from low altitudes in cool climates to above 3,000 m in the tropics, mostly on mineral soil or peat, and are found on riverbanks, beside waterfalls, on steep slopes, in precipitous, small hanging valleys at the head of streams and in extremely rainy, wet regions, sometimes also in dense shade and mossy forests. Gunnera hamiltonii and G. dentata occur in damp sand hollows by the sea and G. herteri grows in seepages of emerging groundwater between coastal dunes (Wanntorp et al. 2003). Gunnera-Nostoc Symbiosis. All species have peculiar organs (often called glands) breaking through the epidermis immediately below very young developing leaves. These organs were identied by Miehe (1924) as arrested adventitious roots (Fig. 62). They produce copious mucilage through which cyanobacteria of the genus Nostoc

gain entrance to the plant stem. Nostoc-infected tissue consists of isolated groups of larger and more rounded cells than those of the ordinary stem parenchyma surrounding them (Fig. 59F, G). In young stems, Nostoc colonies appear as bright blue-green structures. In slightly older parts of the stem, they take on a dark appearance and in even older parts appear as whitish, amorphous masses and are said to be degenerate (Bergman et al. 1992; Wilkinson 2000) Distributional History. Gunnera has an ample microfossil record in the southern hemisphere and parts of the northern hemisphere, dating nearly uninterruptedly back to the early Late Cretaceous (Jarzen 1980; Jarzen and Dettmann 1989; Wanntorp et al. 2004). During Upper Cretaceous and Early Tertiary times, the genus was more widely distributed than it is today. The earliest pollen record attributable to Gunnera (as Tricolpites reticulatus) is from the Turonian of South America; in the Campanian and Maastrichtian, the

Fig. 62. Gunneraceae. Arrested roots infected with Nostoc algae (phycorhizas), occurring in groups of three below the leaf-bases on the axes of Gunnera macrophylla. (Miehe 1924)

Fig. 63. Gunnera magellanica. A Male plant. B Male ower. C Stamen. D Female plant. E Female ower. F Same, vertical section. G Infructescence. H Fruit, vertical section. I Fruit, transverse section. (Schindler 1905)

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genus was represented in Antarctica, New Zealand, continental Australia (from where it is absent today), West Africa and, strangely enough, in North America. In the Palaeogene, the genus appeared additionally in southernmost South America, the Indian Ocean and the Indian Plate. In the Neogene, it retreated southwards in North America (where at present it is represented by a single species in Mexico) and appeared in New Guinea. Wanntorp and Wanntorp (2003) analysed the present distribution of Gunnera within the framework of a cladistic study and the fossil record. Most distributional facts are in agreement with viewing Gunnera as a Gondwana element, which obtained its present distribution mostly by vicariance. However, its widespread and abundant occurrence in North America from the Late Cretaceous to Eocene calls for an additional explanation. Wanntorp and Wanntorp (2003) propose a dispersal event out of South America before the Campanian as leading to the colonization of North America. From there, not only may the Hawaiian islands have been reached by long-distance dispersal but also South America may have been re-colonized by the lineage now corresponding to subg. Panke, where it met with subg. Misandra. Uses. Species of subg. Panke are sometimes used as garden ornamentals; a few of the smaller species are grown in rock-gardens. Gunnera perpensa has been reported to have antifertility and antiabortifacient properties in rats by Mafatle and Joseph (1992). The stems and petioles of Gunnera chilensis are used by indigenous people on a small scale for tanning and dyeing, and petioles are eaten as salad (nalca or rahuay). Only one genus: Gunnera L. Figs. 5963

of single anther. One species, G. herteri Osten, coastal southern Brazil and Uruguay. Subg. Gunnera (= subg. Perpensum [Burman] Schindler). Moderately large herb; rhizome horizontal, intermittently branching, 12 cm thick; bracts and stolons 0, leaves with long petiole, blade cordate or reniform, to 17 28 cm, densely dentate-crenate; young parts pubescent. Inorescence thyrsoid, up to 40 cm long; owers hermaphroditic. One species, G. perpensa L., South Africa to Ethiopia, Madagascar. Subg. Pseudogunnera (Oersted) Schindler. Moderately large-leaved, herb with long stolons; upright stems short, 12 cm diameter; leaves sheathlike at the base, petiole 0.31 m, blade reniform to cordate, irregularly lobed, acutely irregularly sphacelate-dentate and bullate, up to 50 cm wide, with strongly prominent reticulate venation beneath. Inorescences up to 50 cm long, basal owers pistillate with sepals only, apical owers staminate with sepals and petals. One species, G. macrophylla Blume, Malayan archipelago (New Guinea, Solomon Islands, Sulawesi, Java, Sumatra, Borneo and Philippine islands). Subg. Milligania (J.D. Hook.) Schindler. Low stoloniferous, mat-forming herbs; leaves in rosettes on short upright stems, petiole 0.52 cm long, blade orbicular-reniform, subcordate, ovate or elliptic, 13.5(5) cm long. Plants monoecious, usually with staminate and pistillate owers on separate racemes, except in G. monoica Raoul which has bisexual racemes with staminate owers apically. Racemes 15 cm long, pistillate owers with sepals only, staminate owers with sepals and petals. About six species, one from Tasmania, all others from New Zealand. Subg. Misandra (Comm.) Schindler. Low stoloniferous, dioecious herbs (Fig. 63); leaves from short upright stems with ochrea-like scales alternating with the leaves; petiole 225 cm long, blade, reniform or reniform-orbicular, to 11 cm wide indistinctly lobed. Inorescences up to 15 cm, staminate as well as pistillate owers without petals. Differing from subg. Milligania in the possession of ochrea-like scales on shoots. Two species, from Tierra del Fuego and Falkland Islands to Colombia. Subg. Panke (Molina) Schindler. Large to giant, pachycaulous perennials (Fig. 59A) with eshy

Gunnera L., Syst. Nat. ed. 12:587, 598 (Oct. 1767); Mant.: 16, 121 (Oct. 1767); Schindler in Engler, Panzenreich IV, 225:194128 (1905); Mora-Osejo, Flora de Colombia 3:1 178 (1984).

Description as for family; six subgenera: Subg. Ostenigunnera Mattfeld. Diminutive glabrous annual herb; leaf blades to 1.4 cm, abelliform, with up to 20 lobes each ending in a hydathode; indumentum, bracts, stolons and rhizome 0. Inorescences interaxillary, racemes, c. 1 cm long, pistillate owers basally, without perianth, staminate owers apically, often consisting

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stems, up to 3 m long and 40 cm thick, upright, with age often becoming decumbent, rarely branching; youngest parts of stem and terminal bud covered by numerous linear-lanceolate, laciniate or entire, often brightly orange-coloured bracts or scales up to 40 cm long, bearing mucilageproducing glands on the adaxial surface. Petioles up to 2.7 m long, blades mostly palmately lobed (Fig. 59B), from 25 cm up to 3 m in diameter. Inorescences up to 0.5 m compound spikes or racemes (Fig. 59C). Pistillate owers with sepals only, perfect and staminate owers with sepals and petals. About 50 species, South and Central America, Mexico, the Juan Fernandez Islands and Hawaii; G. manicata Linden and G. chilensis Lam. often cultivated in gardens.

Selected Bibliography
Behnke, H.-D. 1986. Contributions to the knowledge of sieve-element plastids in Gunneraceae and allied families. Pl. Syst. Evol. 151:215222. Bergman, B., Johansson, C., Sderbck, E. 1992. The NostocGunnera symbiosis. New Phytol. 122:379400. Beuzenberg, E.J., Hair, J.B. 1963. Contributions to a chromosome atlas of the New Zealand Flora, 5. N. Z. J. Bot. 1:5367. Boutique, R. 1968. Haloragaceae. In: Flore du Congo, du Rwanda et du Burundi. Meise: Jardin Botanique National de Belgique. Dawson, M.I. 1983. Chromosome numbers of three South American species of Gunnera (Gunneraceae). N. Z. J. Bot. 21:457459. Doyle, M.F., Scogin, R. 1988. A comparative phytochemical prole of the Gunneraceae. N. Z. J. Bot. 26:493496. Erdtman, G. 1952. See general references. Fuller, D.G., Hickey, L.T. 2005. Systematics and leaf architecture of the Gunneraceae. Bot. Rev. 7:295353. Hegnauer, R. 1966. See general references. Jarzen, D.M. 1980. The occurrence of Gunnera pollen in the fossil record. Biotropica 12:117123. Jarzen, D.M., Dettmann, M.E. 1989. Taxonomic revision of Tricolpites reticulatus Cookson ex Couper, 1953 with notes on the biogeography of Gunnera L. Pollen Spores 31:97112. Johri, B.M. et al. 1992. See general references. Lowrey, T.K., Robinson, E.R. 1988. The interaction of gynomonoecy, dichogamy, and wind-pollination in Gunnera perpensa L. (Gunneraceae) in South Africa. Monogr. Syst. Bot. Missouri Bot. Gard. 25:237246. Mafatle, T.J.P., Joseph, M.M. 1992. Antifertility and antiabortifacient properties of Gunnera perpensa. In: Abstract Volume South African Association of Botanists 18th Annual Congress, p. 33. Mattfeld, J. 1933. Weiteres zur Kenntniss der Gunnera herteri Osten. Montevideo: Ostenia (Coleccion de Trabajos Botanicos), pp. 102118.

Miehe, H. 1924. Entwicklungsgeschichtliche Untersuchungen der Algensymbiose bei Gunnera macrophylla. Bl. Flora 117:115. Modilewski, J. 1908. Zur Embryobildung von Gunnera chilensis. Ber. Deutsch. Bot. Gesell. 26a: 550556. Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationships among members of the Saxifragaceae sensu lato based on rbcL sequence data. Ann. Missouri Bot. Gard. 80:631660. Netolitzky, F. 1926. Anatomie der Angiospermen-Samen. Berlin: Borntraeger. Pacheco, P., Crawford, D.J., Stuessy, T.F., Silva, O.M. 1993. Flavonoid chemistry and evolution of Gunnera (Gunneraceae) in the Juan Fernandez Islands, Chile. Gayana Bot. 50:1728. Praglowski, J. 1970. The pollen morphology of the Haloragaceae with reference to taxonomy. Grana 10:159 239. Rutishauser, R., Wanntorp, L., Pfeifer, E. 2004. Gunnera herteri developmental morphology of a dwarf from Uruguay and S Brazil (Gunneraceae). Pl. Syst. Evol. 248:219241. Schindler, A.K. 1905. Halorrhagaceae. In: Engler, A. (ed.) Das Panzenreich IV, 225. Leipzig: W. Engelmann, pp. 1133. Skottsberg, C. 1928. Zur Organographie von Gunnera. Svensk Bot. Tidskr. 22:392415. Soltis, D.E. et al. 2000. See general references. Soltis, D.E. et al. 2003. See general references. St. John, H. 1957. Gunnera magnica, a new species from the Andes of Colombia. Svensk Bot. Tidsk. 51:521528. Takhtajan, A. 1997. See general references. Van der Meijden, R., Caspers, N. 1971. Haloragaceae. Flora Malesiana I, 7:239263. Leiden: Noordhoff. Wanntorp, L., Wanntorp, H.-E. 2003. The biogeography of Gunnera L.: vicariance and dispersal. J. Biogeogr. 30:979987. Wanntorp, L., Wanntorp, H.-E., Kllersj, M. 2002. Phylogenetic relationships of Gunnera based on nuclear ribosomal DNA ITS region, rbcL and rps16 intron sequences. Syst. Bot. 27:512521. Wanntorp, L., Wanntorp, H.-E., Rutishauser, R. 2003. On the homology of the scales in Gunnera (Gunneraceae). Bot. J. Linn. Soc. 142:301308. Wanntorp, L., Dettmann, M.E., Jarzen, D.M. 2004. Tracking the Mesozoic distribution of Gunnera: comparsion with the fossil pollen species Tricolpites reticulatus Cookson. Rev. Palaeobot. Palyn. 132:163174. Wanntorp, L., Praglowski, J., Grafstrm, E. 2004. New insight into the pollen morphology of Gunnera (Gunneraceae). Grana 43:1521. Wanntorp, L., Ronse De Graene, L.P. 2005. The Gunnera ower: key to eudicot diversication or response to pollination mode? Intl. J. Plant Sci. 166:945953. Wilkinson, H.P. 2000. A revision of the anatomy of Gunneraceae. In: Rudall, P.J., Gasson, P. (eds) Under the microscope: plant anatomy and systematics. Bot. J. Linn. Soc. 134:233266. Wilkinson, H.P. 1998. Gunneraceae. In: Cutler, D.F., Gregory, M. (eds), Anatomy of the dicotyledons. 2nd edn, Vol. IV. Saxifragales. Oxford: Clarendon Press, 260 272.