gunneraceae

7/27/2019 Gunneraceae

http://slidepdf.com/reader/full/gunneraceae 1/7

GunneraceaeGunneraceae 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 creepingpachycaulous stems, covered with large leaf scars,apically with large to gigantic, long-petioled leavesreaching up to c. 5 m in height (G. magnifica),and between these often covered with conspicuousbracts protecting the inflorescence and vegetative

buds, or stoloniferous and mat-forming, withshort, upright stem portions bearing leaf-rosettes,reaching from 4 cm to about 1 m in height, or inone case (G. herteri), diminutive annuals. Leavesalternate, crowded at stem tips; petioles short tovery long; lamina oblong to reniform or peltate,dentate, crenate or palmately lobed, the crenationsand lobes with protruding hydathodes; venationin large-leaved species palinactinodromous withveins very prominent and projecting as ribson abaxial surface, in smaller-leaved speciesactinodromous or pinnate and less prominent.

Sometimes with more or less conspicuous, simpleto much divided scales between the leaf-bases,stolons with paired, or single ochrea-like, bractsapically. Inflorescences axillary or pseudo-terminal, erect, simple or compound racemes, orspikes; lower flowers mostly pistillate, upper onesstaminate, the middle ones sometimes perfect, orflowers all unisexual, in a few cases plants dioe-cious. Flowers small, bracteate or not, epigynous,sepals 2, anteri-posterior, valvate, sometimes ob-solete, petals 2, transversal, mitre-shaped, slightly

exceeding the sepals, caducous, in female flowerswanting; stamens 2(1), transversal, with shortfilaments; anthers dithecal and tetrasporangiate,opening by longitudinal slits; carpels 2, unitedto form an inferior, unilocular ovary; stylodia 2,transversal; stigmas dry, papillate; ovule solitary,pendulous from apex of locule. Fruit drupaceous,coriaceous to fleshy, oval to globose, green orbright red, rarely white or yellow. Seeds with a very small obcordate embryo embedded in copious,oily endosperm. Specialized organs containingendosymbiontic 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 wetor damp habitats, from low altitudes to above 3,000 m, in South and CentralAmerica, Mexico, Hawaii, Africa, Madagascar, Tas-mania, New Zealand, New Guinea and the Malayanarchipelago

Vegetative Morpholog y. Gunnera comprisesa wide spectrum of growth forms from giant todwarf herbs, usually perennial, with erect or creep-ing stems, often forming mats or clumps by stolonsoriginatingfromleaf axils onthestems andbearingleaf-rosettes apically, or more rarely by branchingof the stems themselves (Figs. 59, 63). The mainstem ofthe dwarf G. herteri is interpreted as a chainof sympodial units each consisting of a leaf andan extra-axillary inflorescence (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, Milliganiaand Misandra. In Pseudogunnera and Milligania,two bud scales at the tip of the stolons precede thefoliage leaves on the erect stem. These cataphyllsare regarded by Wanntorp et al. (2003) to be ho-mologous with a cap-like “ochrea”, which in subg. Misandra occurs on the stolon as well as betweenthe leaves of the upright stem. In subg. Panke, inwhich no stolons are formed, the stems are cov-ered by numerous, large bract-like scales. Skotts-

berg (1928) and Wanntorp et al. (2003) consideralso these scales to be cataphylls.

Vegetative Anatomy. (Information mostly from Wilkinson 1998, 2000). Nodes are multilacu-nar and multitrace. Leaves are bifacial, hypostoma-tous or amphistomatous; stomata are anomocytic.The lower leaf surface has always a smooth waxcover; the cuticle is smooth or (in some speciesof subg. Milligania) finely striate. Marginal leaf hydathodes with an epithem are found in allsubgenera (Fig. 59D), while laminar hydathodes

are restricted to subg. Panke. The leaf axils of Gun-



178 H.P. Wilkinson and L. Wanntorp

nera herteri contain 2–5 inconspicuous glandularcolleters (Rutishauser et al. 2004). Unicellular hairsare widespread and lacking only in G. herteri; otherhair types including uniseriate and multiseriate,stalked andglobular hairs are foundin subg.Panke.Domes of raised silicified cells (“warts”) on the

upper leaf surface and spine-like emergences onpetioles and the larger veins of the lower leaf sur-face are characteristic of subg. Panke (Fig. 59C, E).

The vascular systems of stems and petioles aretypically polystelic. The bundles have the xylemsurrounded by about six portions of phloem (am-phicribal) and are sheathed by a well-defined endo-dermis with Casparian thickenings. In the stems of the pachycaulous, non-stoloniferous subg. Panke,the bundles may amount to several hundred perstem and in subg. Gunnera to about 60. Among

the stoloniferous subgenera, the large-leaved subg.Pseudogunnera and the small-leaved subg. Milliga-nia and Misandra have only few (3–5) larger andsome smaller bundles, the latter to leaves and inflo-rescences. The vascular tissue of the stolons is notpolystelic but siphonostelic (-modified); it consistsof a single tube of xylem and phloem (G. densiflora), or of tubes of internal and external phloemseparated by twotubes of xylem,and is surroundedby an endodermis. Vessel elements are usually very to moderately small; perforation plates in stolonsand roots are mainly scalariform with few to many

bars, andin thestems oflarge-leaved species simpleperforation plates are more common.

Cluster crystals (druses) are widespread in var-ious tissues.

Behnke (1986) found sieve element plastidscontaining protein crystals and starch grains (Pcstype).

Flower Structure. The floral symmetry of Gunnera is most remarkable: the petals, stamensand carpels – at least the stylodia – are located

in the transverse plane (Wantrop and Ronse DeGraene 2005), reminiscent of the position of thesefloral organs in Sabiaceae and, to some degree, inProteaceae.

Fig. 59. Gunneraceae. A–C Gunnera manicata growingin the Royal Horticultural Society’s 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 Aninflorescence (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 adaxialsurface 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 µm. G Heterocysts from F atarrows, scale bar = 10 µm. (Orig. H. Wilkinson)

Embryology. In Gunnera macrophylla andG. chilensis, the pollen grains are two-celled atanthesis. The ovule is anatropous, bitegmic andcrassinucellate, and the micropyle is formed by the inner integument alone. The embryo sac istetrasporic and 16-nucleate (Peperomia-type) and,

apart from the egg and the synergids, contains sixantipodal cells and a group of cells fusing to formthe secondary embryo sac nucleus. Endospermdevelopment is cellular; the suspensor forms nohaustorium (Modilewski 1908).

Pollen Morphology. Pollen of Gunnera isvery distinctive, tricolpate, suboblate spheroidal(Fig. 60), and can be recognised by the fossaper-turate shape with bulging mesocolpia and themicroreticulate exine, usually 20–28 × 25–37 µm

(Erdtman 1952; Praglowski 1970; Jarzen 1980;Wanntorp et al. 2004).

Karyology. Beuzenberg and Hair (1963) re-ported 2n = 34 for Gunnera monoica, G. prorepens,G. densiflora, G. dentata and G. hamiltonii, andseveral hybrids (all in subg. Milligania); the samenumber was counted for various South Americanspecies by Dawson (1983) and Pacheco et al. (1993)

Pollination. Gunnera perpensa shows all at-tributes of wind pollination (the general condi-

tion in the genus), such as high pollen/ovule ratio,strong protandry in the hermaphroditic flowers,and starch storage in pollen (Lowrey and Robinson1988).

Fruit and Seed. The fruit is drupaceous, green-ish-reddish, dry and relatively small (1–2mm long)in subg. Panke, Pseudogunnera and Gunnera, insubg. Misandra and Milligania larger (up to 8 mm

long), and often brightly coloured; G. magellanicais called “frutilla del diablo”, devil’s strawberry.

In the maturing seed, the integuments and nu-cellus disappear, with the exception of the outerepidermis of the outer integument which is madeup of thin-walled cells filled with red sap; mechan-



Gunneraceae 179




Fig. 60. Gunneraceae, pollen grains. A, B, E, F Gunnerachilensis, SEM micrographs. C, D G. macrophylla, light mi-crographs. A Polar view. B, E Equatorial view. C, D Opticalsections showing thickened exine at colpi margins (C) andpoles (D). F Equatorial view of one colpus and reticulateornamentation. A–E ×1,000; F ×51,500. (A, B, E, F Pho-tographs H. Wilkinson; C, D photographs M.M. Harley)

ical protection of the seed is taken over by the peri-carp. The endospermis copious, its cells containingoil, starch and aleurone with crystalloids. The em-

bryo is very small, heart-shaped and lies excentric(Netolitzky 1926).

Phytochemistry. The leaves of Gunnera mani-cata contain high concentrations of an unidentifiedellagitannin (Doyle and Scogin 1988); in G. chilen-sis, the tannin content of the rhizomes amounts to9.3% (Hegnauer 1966). Pacheco et al. (1993) havestudied the flavonoid variation of various SouthAmerican species

Relationships Within the Family. Cladistic

analyses of Gunnera based on nuclear and plastid

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

gene regions by Wanntorp et al. (2002), and Wan-ntorp and Wanntorp (2003) resolved Gunnera asmonophyletic and confirmed the sectional classi-fication proposed by Schindler (1905). Moreover,subg. Ostenigunnera with the diminutive G. herteriwas recovered as sister to all remaining sections,with subg. Gunnera subsequently sister to the re-maining subclades. Figure 61 represents this topol-ogy with an indication of gains and losses of sev-eral characters.Gunnera herteri lacks the polysteliccondition 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 vegetativebranches and inflorescences with the main axis forsome distance above the axil.

Affinities. Gunnera has traditionally beenincluded in Haloragaceae but has often beenelevated to family rank, although its affiliation hasremained uncertain; Takhtajan (1997) includedit in his Saxifraganae. Numerous molecular

studies have now recovered Gunneraceae in closeassociation with Myrothamnaceae in a clade atthe base of the eudicots, more precisely as sisterto all remaining core eudicots (Soltis et al. 2000,2003). A comparison of the characters of Gunneraand Myrothamnus (Wilkinson 2000) shows thatthere exists very little agreement morphologically between the two genera.

Distribution and Habitats. Gunnera ismostly southern hemispheric in distribution, butinSouthandCentralAmerica,theHawaiianislands

and Malesia it extends into low northern latitudes.



Gunneraceae 181

The species prefer wet or damp, cool places fromlow altitudes in cool climates to above 3,000 m inthe tropics, mostly on mineral soil or peat, and arefound on riverbanks, beside waterfalls, on steepslopes, in precipitous, small hanging valleys atthe head of streams and in extremely rainy, wet

regions, sometimes also in dense shade and mossy forests. Gunnera hamiltonii and G. dentata occurin damp sand hollows by the sea and G. herterigrows in seepages of emerging groundwaterbetween coastal dunes (Wanntorp et al. 2003).

Gunnera-Nostoc Symbiosis. All species havepeculiar organs (often called “glands”) breakingthrough the epidermis immediately below very young developing leaves. These organs wereidentified by Miehe (1924) as arrested adventitious

roots (Fig. 62). They produce copious mucilagethrough which cyanobacteria of the genus Nostoc

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

1924)

gain entrance to the plant stem. Nostoc-infectedtissue consists of isolated groups of larger andmore rounded cells than those of the ordinary stem parenchyma surrounding them (Fig. 59F, G).In young stems, Nostoc colonies appear as brightblue-green structures. In slightly older parts of the

stem, they take on a dark appearance and in evenolder parts appear as whitish, amorphous massesand are said to be “degenerate” (Bergman et al.1992; Wilkinson 2000)

Distributional History. Gunnera has an am-ple microfossil record in the southern hemisphereand parts of the northern hemisphere, datingnearly uninterruptedly back to the early Late Cre-taceous (Jarzen 1980; Jarzen and Dettmann 1989;Wanntorp et al. 2004). During Upper Cretaceous

and Early Tertiary times, the genus was morewidely distributed than it is today. The earliestpollen record attributable to Gunnera (as Tricol- pites reticulatus) is from the Turonian of SouthAmerica; in the Campanian and Maastrichtian, the

Fig. 63. Gunnera magellanica. A Male plant. B Male flower.C Stamen. D Female plant. E Female flower. F Same, verticalsection. G Infructescence. H Fruit, vertical section. I Fruit,

transverse section. (Schindler 1905)




genus was represented in Antarctica, New Zealand,continental Australia (from where it is absent to-day), West Africa and, strangely enough, in NorthAmerica. In the Palaeogene, the genus appearedadditionally in southernmost South America, theIndian Ocean and the Indian Plate. In the Neogene,

it retreated southwards in North America (whereat present it is represented by a single species inMexico) and appeared in New Guinea.

Wanntorp and Wanntorp (2003) analysed thepresent distribution of Gunnera within the frame-work of a cladistic study and the fossil record. Mostdistributional facts are in agreement with viewingGunnera as a Gondwana element, which obtainedits present distribution mostly by vicariance.However, its widespread and abundant occurrencein North America from the Late Cretaceous to

Eocene calls for an additional explanation. Wan-ntorp and Wanntorp (2003) propose a dispersalevent out of South America before the Campanianas leading to the colonization of North America.From there, not only may the Hawaiian islandshave been reached by long-distance dispersal butalso South America may have been re-colonizedby the lineage now corresponding to subg. Panke,where it met with subg. Misandra.

Uses. Species of subg. Panke are sometimes usedas garden ornamentals; a few of the smaller species

are grown in rock-gardens. Gunnera perpensa hasbeen reported to have antifertility and antiabor-tifacient properties in rats by Mafatle and Joseph(1992). The stems and petioles of Gunnera chilensisare used by indigenous people on a small scale fortanning and dyeing, and petioles are eaten as salad(“nalca” or “rahuay”).

Only one genus:

Gunnera L. Figs. 59–63

Gunnera L., Syst. Nat. ed. 12:587, 598 (Oct. 1767); Mant.:

16, 121 (Oct. 1767); Schindler in Engler, Pflanzenreich IV,

225:194–128 (1905); Mora-Osejo, Flora de Colombia 3:1–

178 (1984).

Description as for family; six subgenera:

Subg. Ostenigunnera Mattfeld. Diminutiveglabrous annual herb; leaf blades to 1.4 cm,flabelliform, with up to 20 lobes each ending ina hydathode; indumentum, bracts, stolons andrhizome 0. Inflorescences interaxillary, racemes,c. 1 cm long, pistillate flowers basally, without pe-

rianth, staminate flowers apically, often consisting

of single anther. One species, G. herteri Osten,coastal southern Brazil and Uruguay.

Subg. Gunnera (= subg. Perpensum [Burman]Schindler). Moderately large herb; rhizomehorizontal, intermittently branching, 1–2 cm

thick; bracts and stolons 0, leaves with longpetiole, blade cordate or reniform, to 17 × 28 cm,densely dentate-crenate; young parts pubescent.Inflorescence thyrsoid, up to 40 cm long; flowershermaphroditic. One species, G. perpensa L.,South Africa to Ethiopia, Madagascar.

Subg. Pseudogunnera (Oersted) Schindler. Mod-erately large-leaved, herb with long stolons; up-right stems short, 1–2 cm diameter; leaves sheath-like at the base, petiole 0.3–1 m, blade reniform

to cordate, irregularly lobed, acutely irregularly sphacelate-dentate and bullate, up to 50 cm wide,with strongly prominent reticulate venation be-neath. Inflorescences up to 50 cm long, basal flow-ers pistillate with sepals only, apical flowers stami-nate with sepals and petals. One species, G. macrophylla Blume, Malayan archipelago (New Guinea,Solomon Islands, Sulawesi, Java, Sumatra, Borneoand Philippine islands).

Subg. Milligania (J.D. Hook.) Schindler. Low stoloniferous, mat-forming herbs; leaves in

rosettes on short upright stems, petiole 0.5–2 cmlong, blade orbicular-reniform, subcordate, ovateor elliptic, 1–3.5(5) cm long. Plants monoecious,usually with staminate and pistillate flowers onseparate racemes, except in G. monoica Raoulwhich has bisexual racemes with staminate flowersapically. Racemes 1–5 cm long, pistillate flowerswith sepals only, staminate flowers with sepals andpetals. About six species, one from Tasmania, allothers from New Zealand.

Subg. Misandra (Comm.) Schindler. Low stolonif-erous, dioecious herbs (Fig. 63); leaves from shortupright stems with ochrea-like scales alternatingwith the leaves; petiole 2–25 cm long, blade,reniform or reniform-orbicular, to 11 cm wideindistinctly lobed. Inflorescences up to 15 cm,staminateaswellaspistillateflowerswithoutpetals.Differing from subg. Milligania in the possessionof ochrea-like scales on shoots. Two species, fromTierra del Fuego and Falkland Islands to Colombia.

Subg. Panke (Molina) Schindler. Large to giant,

pachycaulous perennials (Fig. 59A) with fleshy



Gunneraceae 183

stems, up to 3 m long and 40 cm thick, upright,with age often becoming decumbent, rarely branching; youngest parts of stem and terminalbud covered by numerous linear-lanceolate, ±laciniate or entire, often brightly orange-colouredbractsorscalesupto40 cm long, bearing mucilage-

producing glands on the adaxial surface. Petiolesup to 2.7 m long, blades mostly palmately lobed(Fig. 59B), from 25 cm up to 3 m in diameter.Inflorescences up to 0.5 m compound spikes orracemes (Fig. 59C). Pistillate flowers with sepalsonly, perfect and staminate flowers with sepalsand petals. About 50 species, South and CentralAmerica, Mexico, the Juan Fernandez Islands andHawaii; 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 fam-ilies. Pl. Syst. Evol. 151:215–222.

Bergman, B., Johansson, C., Söderbäck, E. 1992. TheNostoc-Gunnera symbiosis. New Phytol. 122:379–400.

Beuzenberg, E.J., Hair, J.B. 1963. Contributions to a chro-mosome atlas of the New Zealand Flora, 5. N. Z. J. Bot.1:53–67.

Boutique, R. 1968. Haloragaceae. In: Flore du Congo, duRwanda et du Burundi. Meise: Jardin Botanique Na-

tional de Belgique.Dawson, M.I. 1983. Chromosome numbers of three SouthAmerican species of Gunnera (Gunneraceae). N. Z. J.Bot. 21:457–459.

Doyle, M.F., Scogin, R. 1988. A comparative phytochemicalprofile of the Gunneraceae. N. Z. J. Bot. 26:493–496.

Erdtman, G. 1952. See general references.Fuller, D.G., Hickey, L.T. 2005. Systematics and leaf archi-

tecture of the Gunneraceae. Bot. Rev. 7:295–353.Hegnauer, R. 1966. See general references.Jarzen, D.M. 1980. The occurrence of Gunnera pollen in the

fossil record. Biotropica 12:117–123.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 Spores31:97–112.Johri, B.M. et al. 1992. See general references.Lowrey, T.K., Robinson, E.R. 1988. The interaction of

gynomonoecy, dichogamy, and wind-pollination inGunnera perpensa L. (Gunneraceae) in South Africa.Monogr. Syst. Bot. Missouri Bot. Gard. 25:237–246.

Mafatle,T.J.P., Joseph,M.M. 1992.Antifertility and antiabor-tifacient properties of Gunnera perpensa. In: AbstractVolume South African Association of Botanists 18thAnnual Congress, p. 33.

Mattfeld, J. 1933. Weiteres zur Kenntniss der Gunnera hert-eri Osten. Montevideo: Ostenia (Coleccion de TrabajosBotanicos), pp. 102–118.

Miehe, H. 1924. Entwicklungsgeschichtliche Untersuchun-gen der Algensymbiose bei Gunnera macrophylla. Bl.Flora 117:1–15.

Modilewski, J. 1908. Zur Embryobildung von Gunnerachilensis. Ber. Deutsch. Bot. Gesell. 26a: 550–556.

Morgan, D.R., Soltis, D.E. 1993. Phylogenetic relationshipsamong members of the Saxifragaceae sensu lato based

on rbcL sequence data. Ann. Missouri Bot. Gard.80:631–660.

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 (Gun-neraceae) in the Juan Fernandez Islands,Chile. GayanaBot. 50:17–28.

Praglowski, J. 1970. The pollen morphology of the Halor-agaceae with reference to taxonomy. Grana 10:159–239.

Rutishauser, R., Wanntorp, L., Pfeifer, E. 2004. Gunneraherteri – developmental morphology of a dwarf fromUruguay and S Brazil (Gunneraceae). Pl. Syst. Evol.

248:219–241.Schindler, A.K. 1905. Halorrhagaceae. In: Engler, A. (ed.)

Das Pflanzenreich IV, 225. Leipzig: W. Engelmann, pp.1–133.

Skottsberg, C. 1928. Zur Organographie von Gunnera.Svensk Bot. Tidskr. 22:392–415.

Soltis, D.E. et al. 2000. See general references.Soltis, D.E. et al. 2003. See general references.St. John, H. 1957. Gunnera magnifica, a new species from

the Andes of Colombia. Svensk Bot. Tidsk. 51:521–528.Takhtajan, A. 1997. See general references.Van der Meijden, R., Caspers, N. 1971. Haloragaceae. Flora

Malesiana I, 7:239–263. Leiden: Noordhoff.Wanntorp, L., Wanntorp, H.-E. 2003. The biogeography

of Gunnera L.: vicariance and dispersal. J. Biogeogr.30:979–987.Wanntorp, L., Wanntorp, H.-E., Källersjö, M. 2002. Phy-

logenetic relationships of Gunnera based on nuclearribosomal DNA ITS region, rbcL and rps16 intron se-quences. Syst. Bot. 27:512–521.

Wanntorp, L., Wanntorp, H.-E., Rutishauser, R. 2003. Onthe homology of the scales in Gunnera (Gunneraceae).Bot. J. Linn. Soc. 142:301–308.

Wanntorp, L., Dettmann, M.E., Jarzen, D.M. 2004. Track-ing the Mesozoic distribution of Gunnera: compar-sionwiththefossilpollenspecies Tricolpites reticulatusCookson. Rev. Palaeobot. Palyn. 132:163–174.

Wanntorp, L., Praglowski, J., Grafström, E. 2004. New in-

sight into the pollen morphology of Gunnera (Gun-neraceae). Grana 43:15–21.Wanntorp, L., Ronse De Graene, L.P. 2005. The Gunnera

flower: key to eudicot diversification or response topollination mode? Intl. J. Plant Sci. 166:945–953.

Wilkinson, H.P. 2000. A revision of the anatomy of Gunner-aceae. In: Rudall, P.J., Gasson, P. (eds) Under the mi-croscope: plant anatomy and systematics. Bot. J. Linn.Soc. 134:233–266.

Wilkinson, H.P. 1998. Gunneraceae. In: Cutler, D.F., Gre-gory, M. (eds), Anatomy of the dicotyledons. 2nd edn,Vol. IV. Saxifragales. Oxford: Clarendon Press, 260–272.

gunneraceae

Documents