The Thalli that are Green (Taxon of the Week: Lemnoideae)

The Araceae is the family of plants including such widely-grown species such as calla lilies and taro. Among other things, the family is famous for including some of the largest floral structures in the world. What is perhaps less widely appreciated is that it also includes some of the smallest and also some of the strangest flowering plants of all*.

*The very strangest flowering plants are the Podostemoideae, but I'll save them for another day.


Wolffia arrhiza, one of the world's smallest flowering plants. Each separate dot is an individual plant. Photo by Christian Fischer.

Duckweeds are the minute plant that can be found growing in large numbers on many still bodies of water. The main body of the plant is a flattened, often oval thallus (not a leaf but rather a highly reduced and fused leaf and stem). In three of the recognised genera of duckweeds, Lemna, Spirodela and Landoltia (the 'Lemneae'), one or more short roots emerge from one end of the thallus (the proximal end). In the other two genera, Wolffia and Wolffiella (the Wolffieae), the thallus lack roots. The vascular system is greatly reduced in 'Lemneae' and almost entirely absent in Wolffieae. Much of the thallus is occupied by gas-filled spaces that keep it buoyant (Hillman, 1961). The proximal end of the thallus also bears pockets on the underside from which daughter thalli grow vegetatively or in which the flower develops. The 'Lemneae' possess two such pockets, one on each side, while the Wolffieae possess only a single pocket. The entire plant is generally less than five millimetres (the size reached by Landoltia punctata) while Wolffia individuals are less than half a millimetre long when mature. Phylogenetic analysis indicates that the 'Lemneae' are paraphyletic; Lemna, which is smaller than Spirodela and Landoltia with only a single rooth per thallus, is sister to the even more reduced Wolffieae (Les et al., 2002).


Spirodela (large thalli), Lemna (smaller thalli) and Wolffia (minute thalli). Photo by G. D. Carr.

The flowers of duckweed are correspondingly tiny and many species produce them only rarely with vegetative reproduction being the primary means of multiplication (Hillman, 1961). Daughter thalli may begin producing their own daughters before separating from the parent, leading to the production of small colonies. Individuals of the double-pocketed 'Lemneae' demonstrate 'handedness' in their growth; in a new thallus grown from seed, either the right- or left-hand pocket may be the 'plus' pocket from which the first daughter thallus grows, but all successive vegetatively produced thalli will grow their own first daughter thallus on the same side as their parent did. If a flower is produced (and each individual thallus will only ever flower once) then it will always grow on the other side in the 'minus' pocket. It is a bit of an open (and somewhat academic) question whether duckweeds produce a single hermaphroditic flower or separate male and female flowers, as there are no petals or sepals, but the important detail is that a thallus produces a single pistil and one to three stamens (usually two in 'Lemneae', only ever one in Wolffieae; Wolffieae also only possess a single ovule while 'Lemneae' may possess up to six) which project above the surface of the thallus. The pistil matures before the stamens but may remain receptive until after the stamens open so at least some duckweeds are capable of self-pollination. The exact mode of pollen transport is uncertain: pollen may be carried by wind or water but transport by small insects has also been proposed. Seeds are capable of surviving periods of drying out; many species of duckweed are also capable of producing a dormant form called a turion, a modified, thicker thallus that lacks the air spaces of a normal thallus and possesses a dense load of starch grains instead.


Thick growth of Landoltia punctata. Photo by A. Murray.

Though most authors have regarded them as a separate family, the Lemnaceae, a relationship between duckweeds and Araceae has been popular since the 1800s. The main connecting link has been through comparison with the floating aroid Pistia stratiotes which resembles duckweed both in its general lifestyle and in the production of its flowers in basal pockets. Some authors have even proposed including Pistia in the Lemnaceae and the Palaeocene fossil plant Limnobiophyllum (with reduced floating rosettes) has been suggested as a morphological link between the two (Stockey et al., 1997). Molecular studies, while supporting a nested position for duckweeds within Araceae (which is why I refer to them as subfamily Lemnoideae), have not supported a direct relationship between duckweeds and Pistia (Rothwell et al., 2004); however, duckweeds show much greater branch lengths than other Araceae.

REFERENCES

Hillman, W. S. 1961. The Lemnaceae, or duckweeds: a review of the descriptive and experimental literature. Botanical Review 27 (2): 221-287.

Les, D. H., D. J. Crawford, E. Landolt, J. D. Gabel & R. T. Kimball. 2002. Phylogeny and systematics of Lemnaceae, the duckweed family. Systematic Botany 27 (2): 221-240.

Rothwell, G. W., M. R. Van Atta, H. E. Ballard Jr & R. A. Stockey. 2004. Molecular phylogenetic relationships among Lemnaceae and Araceae using the chloroplast trnL–trnF intergenic spacer. Molecular Phylogenetics and Evolution 30 (2): 378-385.

Stockey, R. A., G. L. Hoffman & G. W. Rothwell. 1997. The fossil monocot Limnobiophyllum scutatum: resolving the phylogeny of Lemnaceae. American Journal of Botany 84 (3): 355-368.

Name the Bug: Pistia stratiotes

Pistia stratiotes. Photo by Bhushan Dalvi.

As two readers correctly surmissed, the main subject of this photo is the aroid Pistia stratiotes, commonly known as water lettuce. While the specimens shown here appear to have become stranded, water lettuce grows as free-floating rosettes on the surface of open bodies of water. The leaves radiate from an extremely shortened central stem with the tiny flowers produced in pockets at the bases of the leaves. As well as producing flowers, water lettuce reproduces vegetatively by the production of lateral stolons that give rise to daughter rosettes. Given time, a colony of water lettuce can carpet an entire lake.

I said that this ID was a clue to the next Taxon of the Week. Pistia stratiotes is not the only floating member of the Araceae: the remaining examples will be the subject of the next post.

Taxon of the Week: Rhaphidophora

Rhaphidophora decursiva growing in the Sydney Botanical Gardens. Photo by Tony Rodd.

As currently recognised, Rhaphidophora is a large genus of about 100 species of lianes (woody climbers) of the family Araceae found in the tropics of the Old World from Africa to northern Australia. Rhaphidophora forms part of the tribe Monstereae whose most familiar member is probably Monstera deliciosa, the Swiss cheese plant of many a garden, and the flowers and fruit of Rhaphidophora are similar to those of Monstera. Some Rhaphidophora species have pinnate or perforated leaves while others have entire leaves. Most Rhaphidophora species do not seem to currently have a great deal of economic significance except as ornamental plants though a small number have been investigated in recent years for their pharmacological properties. Rhaphidophora pertusa stems are chopped up and mixed with rice gruel before being fed to cattle or buffaloes in India to induce oestrus (Santosh et al., 2006).


Rhaphidophora foraminifera. Photo by Eric in SF.

The genera of the Monstereae such as Rhaphidophora, Monstera and Epipremnum have not had their definitions substantially revised since 1908 and are currently regarded by many authors as problematic. They have been primarily distinguished on the basis of reproductive anatomy (Rhaphidophora, for instance, has numerous ovules, punctate stigmas and minute albuminous seeds) but reproductive characters are often at odds with vegetative characters (Hay, 1993) and a revision of the group is overdue (matters were not helped by the suggestion - since shown to be mistaken - that Rhaphidophora and Epipremnum shared the same type species). A molecular study by Tam et al. (2004) also identified polyphyly of Rhaphidophora, with the majority of Rhaphidophora species forming a single clade but a significant minority forming clades with species of other genera.

REFERENCES

Hay, A. 1993. Rhaphidophora petrieana - a new aroid liane from tropical Queensland; with a synopsis of the Australian Araceae-Monstereae. Telopea 5 (2): 293-300.

Santosh, C. R., N. B. Shridhar, K. Narayana, S. G. Ramachandra & S. Dinesh. 2006. Studies on the luteolytic, oestrogenic and follicle-stimulating hormone like activity of plant Rhaphidophora pertusa (Roxb.). Journal of Ethnopharmacology 107 (3): 365-369.

Tam, S.-M., P. C. Boyce, T. M. Upson, D. Barabé, A. Bruneau, F. Forest & J. S. Parker. 2004. Intergeneric and infrafamilial phylogeny of subfamily Monsteroideae (Araceae) revealed by chloroplast trnL-F sequences. American Journal of Botany 91 (3): 490-498.

Flowers in the Water (Taxon of the Week: Hydrocharitaceae)

Hydrocharis morsus-ranae, frogbit (and is there anyone out there who can tell me why this plant is called "frogbit"?), an insect-pollinated example of Hydrocharitaceae. Photo by J. R. Crellin.

The Hydrocharitaceae is a small but morphologically diverse family of fully aquatic monocots. About eighty species are included in about fifteen genera, excluding the genus Najas which has occasionally been suggested to belong in this family (Tanaka et al., 1997). Hydrocharitaceae includes both freshwater and marine species, such as seagrasses (Enhalus, Thalassia and Halophila), eelgrasses (Hydrilla, Vallisneria) and oxygen weeds (Egeria, Elodea, Lagarosiphon). Depending on the species, Hydrocharitaceae may live their lives partially or entirely submerged.

A major factor in the diversity of this family derives from the diversity of pollination methods. Hydrocharitaceae may be monoecious (separate male and female flowers, but on the one plant) or dioecious (separate male or female plants). Many of the genera in this family are insect-pollinated (entomophilous), with flowers protruding from the water, and comparison with related families suggests that this is the ancestral condition for the family. However, more that one lineage of Hydrocharitaceae has evolved to take advantage of their home environment by becoming water-pollinated (hydrophilous). Such species may be epihydrophilous, with flowers borne at the water surface, or hypohydrophilous, with flowers completely underwater. The genera Vallisneria, Lagarosiphon, Nemachandra and Enhalus have become epihydrophilous in a way that no other aquatic flowering plant has - rather than releasing pollen into the water like other hydrophilous plants, the entire male flower is released to float on the surface of the water until it reaches a female flower. Remarkably, while this process is unique to Hydrocharitaceae, genera with detaching flowers do not form a single clade - instead, the process has evolved at least three times within the Hydrocharitaceae (Tanaka et al., 1997, who did not test the position of Nemachandra).


Inflorescence of the seagrass Enhalus acoroides, and a floating congregation of the small detached male flowers. Photo from Team Seagrass.

Hydrocharitaceae also have other reproductive options open to them. Vegetative reproduction is common among plants, a factor which gardeners have profited from for generations. The Hydrocharitaceae are vegetative reproducers par excellence, with broken-off fragments all too ready to reroot and establish themselves. In the case of the Florida seagrass Halophila johnsonii, the only marine plant listed as endangered in the United States, vegetative reproduction may be the only thing keeping it going. Only female flowers have ever been recorded for this species, and seed production has never been recorded. While some have suggested that Halophila johnsonii may reproduce apomictically (parthenogenetically for the zoologically-inclined), York et al. (2008) demonstrated that this is probably not the case - ovules and gametes are produced in the same manner as other sexually-reproducing Halophila species. Theoretically, pollination of these ovules should be entirely possible - but somehow, the males have all disappeared, and the Halophila johnsonii females are waiting for a pollinator that will never come.


Elodea canadensis, one of the fully submerged "oxygen weeds" widely used in fish tanks, from whence they escape to take over the world. Photo by Ondřej Zicha.

Unfortunately, this propensity for vegetative propagation is also the dark side of Hydrocharitaceae. Widely propagated as aquatic ornamentals or for aquaria and fish tanks, Hydrocharitaceae have found it all too easy to escape their alloted positions and invade exotic waterways. In New Zealand, three species of oxygen weed (Egeria densa, Lagarosiphon major and Elodea canadensishave become leading invasives, despite the fact that, for all three, individuals of almost invariably only a single sex are present in the wild, rendering sexual reproduction nonexistent (Healy & Edgar, 1980). In 1968, power production at a hydroelectric station on the Waikato River was brought to a halt by dense Lagarosiphon major blocking the station's water intake. Elodea canadensis achieved even greater invasions:

The heavy stand in Lake Rotoroa, Nelson Lakes National Park is noteworthy: between 1965 and 1971 the plant formed a virtually complete marginal weed-bed to a depth of 8.5 m, with stems to 6 m high. Here, in terms of dry matter per m², the amount of weed herbage is significantly higher than that recorded for any other freshwater macrophyte community elsewhere in the world. (Healy & Edgar, 1980)

REFERENCES

Healy, A. J., & E. Edgar. 1980. Flora of New Zealand vol. III. Adventive cyperaceous, petalous and spathaceous monocotyledons. P. D. Hasselberg, Government Printer: Wellington (New Zealand).

Tanaka, N., H. Setoguchi & J. Murata. 1997. Phylogeny of the family Hydrocharitaceae inferred from rbcL and matK gene sequence data. Journal of Plant Research 110 (3): 329-337.

York, R. A., M J. Durako, W. J. Kenworthy & D. W. Freshwater. 2008. Megagametogenesis in Halophila johnsonii, a threatened seagrass with no known seeds, and the seed-producing Halophila decipiens (Hydrocharitaceae). Aquatic Botany 88: 277-282.