Download The Flowers, Fruits, and Seeds of Thalassia

THE FLOWERS, FRUITS, AND SEEDS OF
THALASSIA
TESTUDINUM
KOENIG'
PHILIP A. ORPURT AND LINDA L. BORAL2
Manchester College, North Manchester, Indiana
ABSTRACT
The flowers of turtle-grass, Thalassia testudinum Konig, are redescribed
from specimens collected in Biscayne Bay, Florida. An account is given
of fruit development and structure. Anatomy of the seed and germination
of this plant are described for the first time.
INTRODUCTION
The herbaceous flowering plant known as turtle-grass, Thalassia testudinum Konig (Fig. 1), is found in extensive submarine beds throughout
the Caribbean and the Gulf of Mexico (Humm, 1956; Thorne, 1954).
The plant occurs along both coasts of Florida and is particularly abundant
in the vicinity of Biscayne Bay, where it is considered
to be of ecological
importance as a primary producer of carbohydrate in tropical waters
(Voss & Voss, 1955). Its distribution in the United States and some
aspects of its ecology have been discussed by D. R. Moore (1963).
Our attention was attracted to Thalassia in the early spring of 1963
when a previously undescribed fungus was isolated from necrotic lesions
on the leaves of the plant. While acquainting ourselves with T. testudinum,
its life history, floral structure, fruit formation, and seed structure and
germination, it became apparent that there was a considerable lack of information on these important aspects of the plant. Thalassia testudinum is one
of only a few true marine angiosperms. It produces submerged flowers,
undergoes pollination, forms fruit, and accomplishes seed germination
while remaining totally submerged in saIt water. Plants such as Thalassia,
pollinated beneath the water, are termed "hydrophilous." This adaptation
represents an advancement relative to an aquatic environment found in
few hydrophytes (Arber, 1920).
According to Rydberg (1909), the first description of T. testudinum
by Konig as a flowering plant in Konig and Sims, "Annals of Botany"
in 1906, was based on staminate flowers only. Grisebach (1864) placed
Thalassia in the Naiajadaceae and noted that pistillate flowers were unknown. Small (1903) in his treatise, "Flora of the Southeastern United
States," placed Thalassia in the Hydrocharitaceae, where it is now classified, and like Grisebach was unable to give a description of the pistillate
flowers of this common marine flowering plant. One is not surprised.
'Contribution
No. 542 from The Marine Laboratory.
Institute of Marine Science, University
of Miami. Supported in part by project No. 103-305, Microbiology Branch, Office of Naval
Research, and by US PHS Grant No. 5489.
2N.S.F. Undergraduate
Research Participant.
1964]
Orpurt & Boral: Thalassia Testudinum Konig
297
therefore, at the expressed elation of Rydberg (1909) when he writes,
"One of the most interesting plants recently collected by Mr. Percy Wilson ... on his trip to the Bahamas, was the turtle-grass, Thalassia testudinum, in flowers and young fruit." From this material given him by
Wilson, Rydberg described the pistillate flower and a young fruit of the
plant.
The descriptions and the accompanying diagrams by Rydberg have
since been quoted and copied (Lawrence, 1951; Muenscher, 1944; Small,
1933) as an accurate report on the floral and fruit structure of the plant.
But our observations of these structures of T. testudinum conducted during
the spring and summer of 1963 on material from Biscayne Bay, Florida,
have indicated discrepancies in these published descriptions. In addition to
these observations, an account is given of the adaptations of the fruits
and germinating seeds to their role in the ecology of this plant.
DESCRIPTION
OF FLOWERS
The plants of Thalassia are dioecious, the unisexual flowers developing
in early April and continuing through September in the Miami area. The
earliest bloom is the largest although ordinarily fewer than 1 per cent of
the total plants in a bed are in flower at a given time. The shorter plants
in the shallower beds flower earliest followed by those in the deeper beds
as the season progresses.
Although most turtle-grass beds are composed of either male or female
plants (Phillips, 1960), at Matheson Hammock, in Biscayne Bay, they
occur intermixed in approximately equal numbers.
The staminate flower of T. testudinum is essentially as described previously (Rydberg, 1909). It consists of 9 nearly sessile, basifixed, 4-thecate
anthers closely appresed and surrounded by a perianth of three elliptical
to oval segments (Figs. 4, 5). The perianth may be colorless or in some
specimens lightly marked with pink to violet spots or small streaks. The
pedicel and bud is enclosed by the 2-cleft spathe, but the anthers, when
mature, project beyond the spathe as the pollen is freed into the water.
Each theca of the anther is occupied by a mass of pollen (Fig. 8).
The thecae dehisce by means of a vertical slit (Fig. 6) through which
the pollen escapes attached together in long mucilaginous strands (Fig. 9).
Individual grains are spherical, 50-60 JL in diameter, appear granular
internally, and are hyaline (Fig. 7). The exine is spinulose and there
are no germ pores or furrows.
The pistillate flower is nearly sessile within a 2-c1eft spathe (Figs. 2, 3).
There is a simple, inferior ovary (Fig. 10) containing usually 1 to 3
(rarely more) ovules in individual locules (Figs. 11, 12). The style,
projecting above the ovary, is a tube similar in structure to that described
in Halophila ovalis by Balfour (1878). It is filled with mucilage (Fig.
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Bulletin of Marine Science of the Gulf and Caribbean
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c'; :,::/-
11'1',,:
b
II,'
5
6
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-,
c
b
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17
19
20
FIGURES 1-20. Thalmsia testudinum Konig. 1, Habit: a, blade; b, decomposing
blades; c, rhizome; d, root.-2,
2 flower: a, bud; h, spathe; c, inferior
ovary.-3,
2 flower: a, stigmas; h, perianth; c, ovary; d, spathe.-4,
0
flower: a, bud; b, spathe.-5,
0 flower: a, stamen; b, perianth; c, spathe.-6,
Stamen.-7,
Pollen grain.-8,
Stamen, x section: a, microsporangium;
h,
theca.-9,
Pollen strand: a, grain; b, mucilage.-lO,
Sectioned 2 flower: a,
stigma; b, style element; c, cycle of styles; d, segments of perianth; e, core of
style tube; f, style tube; g, hypanthium; h, ovary.-11,
Longitudinal section
1964]
Orpurt & Baral: Thalassia Testudinum
Konig
299
IOe) and is nearly equal to the ovary in length (Fig. lOt). There are
three perianth segments spreading from the apex of the stylar tube
(Fig. I Od). From the base on the inside of the perianth segments, 7 or
8 stylar elements arise. Each of the elements divides into two stigmas
(Fig. I Oa,b). Thus, contrary to the reported 9 to 12 stigmas (Rydberg, 1909), there are usually 14 or 16 stigmas. The stylar elements and
the perianth are quite fragile, breaking away easily, and it is likely that
the specimens examined by Rydberg were so damaged in transit that an
accurate description was not possible. In any case, it is apparent that the
number of stigmas is greater than reported by Rydberg.
The perianth segments of the pistillate flower, as in the staminate flower,
are commonly spotted or streaked by pink to violet pigment.
The first observed change in the female flower following pollination
is the loss of the stylar elements, which break off at their bases. The
perianth also soon drops off leaving an apical prolongation or beak attached to the ovary (Fig. 11 a) .
DEVELOPMENT
OF FRUIT
The mature fruit of T. testudinum is an elliptical to globose capsule,
20-25 mm wide by 15-20 mm high, with a beak of 3-7 mm (Fig. 13).
As the fruit matures it completely fills and splits the enclosing spathe.
The surface of the fruit is at first echinate, becoming tuberculate
at
maturity. As it ripens, the fruit softens and changes from a bright green
to a yellow-green. Occasional mature fruits are red. The mature fruit may
remain attached to the mother plant, where it dehisces, or it may break
free during heavy wave action. Free fruits remain afloat, thus affording
an excellent means of dispersal. Fruits from the earliest flowers mature
in about 8 weeks at which time dehiscence results in the formation of
5 to 8 irregular valves (Fig. 14). Within the fruit there occur usually 3
seeds (Fig. 12), occasionally 1 or 2, and rarely up to 6. Rydberg (1909)
states that the seeds are numerous. Our observations do not confirm his
report for in no case have we found a fruit with numerous seeds. It is
our opinion that this discrepancy
stems from the fact that Rydberg
of fruit: a, beak; b, pericarp; c, placenta; d, seed.-12, Cross section of fruit:
a, tuberculate exocarp; b, seed coat; c, seed; d, pericarp.-13,
Mature fruit:
a, beak (remains of style tube); b, tuberculate fruit surface; c, spathe.-14,
Dehiscent capsule: G, style; b, valve.-15,
Cotyledon cell: G, wall; b, starch
grain.-16,
Seed: G, chalaza; h, plumule; c, cotyledon.-17,
Seedling: G, leaf;
h, scale; c, chalaza.-18,
Seedling: G, leaf; h, scale; c, root hairs.-19, Seedling:
a, chalaza; b, leaf; c, scale; d, epicotyl; e, radicle; j, vascular strand of cotyledon.-20,
Lower surface of embryo: G, cell with starch grains; b, cell with
tannin: c, root hair.
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Bulletin of Marine Science of the Gulf and Caribbean
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had for study only one immature fruit, in very poor condition. To quote
Rydberg, "The writer intended to make a more careful investigation of
the morphological structure of the fruit, but the dry material, more or
less crushed and distorted by pressing, could not be restored to its original
condition and the sections were as a whole unsatisfactory" (italics ours).
Since the seeds contain numerous starch granules, and since his material
was crushed, it appears very likely that Rydberg mistook the hard starch
granules for the numerous seeds he reports as characteristic of T. testudinum.
STRUCTURE
AND GERMINATION
OF
SEEDS
The inner layer of the pericarp becomes mucilaginous as the fruit
ripens. The seed coat, loosely surrounding the embryo, also becomes
viscid and slips off easily to release the embryo into the water. While the
fruits of Thalassia float, the seeds (embryos) sink immediately upon
release from the fruit, settling with the flat side down. The pyriform seeds
average 10mm in width by 8mm in height (Fig. 16). With the flattened
side down, the chalazal end of the embryo is pointed upward so that
the emerging plumule (Figs. 16b; 17a) is also directed upward. The
plumule, at first enclosed in three scale leaves (Figs. 17b; 18b), may
actually begin to emerge from the seed coat prior to the opening of the
valves of the fruit. After the seed is released from the fruit, and following anchorage by root hair formation and plumule emergence. the young
rhizome emerges and gives rise at the nodes to secondary roots (Figs.
lc; Id).
The germinating embryo exhibits an interesting mechanism by which
it readily becomes anchored in the bottom sand. A large number of root
hairs develop from the lower, flattened (cotyledon) side (Figs. 18c; 20c).
The root hairs develop within 3 days after the seeds settle to the bottom,
and thus quickly anchor the young plant on the unstable substrat~. This
manner of root hair formation and anchorage mechanism is similar to
that reported for Elatine hexandra and Zannichellia polycarpa (Arber,
1920) .
A longitudinal section through the axis of the embryo reveals the internal
organization of the embryo. The vascular axis and the cotyledonary node
forms what may be roughly described as an S (Figs. 19d,f). The radicle
is directed laterally (Fig. 1ge) and is nearly surrounded by the single,
flattened cotyledon. It is the flattened cotyledon consisting of large cells
filled with heavy starch granules (Fig. 15) which forms the base of the
embryo as it comes to rest on the bottom in the water. Some of the
epidermal cells of the cotyledon are darkened with tannin deposits while
others give rise to the root hairs.
1964]
Orpurt & Boral: Thalassia Testudinum Konig
301
SUMMARY
A redescription of the unisexual flowers of T. testudinum Konig, based
upon material from Matheson Hammock, Biscayne Bay, Florida, is given.
Observations on flowering and fruit development indicates that it takes
approximately 8 weeks from the time of pollination for fruits to mature.
Contrary to a statement by Rydberg that Thalassia fruits contain numerous seeds, we found that the usual number is 3. Fruits with more
than 3 seeds were rare.
The pyriform seeds and their germination are described for the first
time. Thalassia fruits float and thereby serve as an excellent means of
plant dispersal. The seeds sink upon their release from the mature capsule,
with their flattened cotyledon side oriented downward. This particular
orientation is due to the formation of numerous starch granules in the
cotyledon cells. Such an orientation thus directs the plumule upward and
at the same time numerous root hairs from the lower, flattened side of
the cotyledon quickly anchor the young plant in the unstable sand Oll
the bottom.
ACKNOWLEDGEMENTS
The authors express their gratitude to Dr. Leonard Greenfield of the
Institute of Marine Science, University of Miami, for his helpful advic~
with this study and for his able assistance in the collection of field data
and materials. Our gratitude is also extended to Dr. S. P. Meyers for his
counsel and assistance in the preparation of the manscript.
SUMARIO
DE Thalassia testudinum KONIG
En el area de Miami las f10res unisexuales de Thalassia testudinum se
presentan mezcladas en lechos submarinos, desde Abril a Septiembre.
Aproximadamente el 1 % de las plantas de un lecho florecen a la vez,
cmpezando desde los Iechos mas bajos hacia los mas profundos, a medida que progresa la estaci6n.
Aunque la flor estaminada es esencialmente como se ha descrito por
autores anteriores, se encontr6 que en la flor pistilada hay usual mente 14
6 16 estigmas en vez de 9 6 12 que es 10 reportado anteriormente. Toma
alrededor de 8 semanas desde el momenta de la polinizaci6n para que las
frutas maduren.
La dehiscencia resulta de la formaci6n de 5 a 8 valvas irregulares.
Contrario a 10 dicho por Rydberg de que las frutas de Thalassia contienen numerosas semillas, nosotros encontramos que el numero usual
es 3. Mas de 3 semillas es cosa muy rara.
Se describen por primera vez, las semillas piriformes y su germinaci6n.
Las frutas de Thalassia flotan, resultando un excelente medio de dispersi6n de la planta. Las semillas se hun den al liberarse de la capsula de la
LAS
FLORES,
FRUTAS
Y SEMILLAS
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Bulletin of Marine Science of the Gulf and Caribbean
(J 4(2)
fruta madura, con el lado lisa del cotiled6n orientado hacia abajo. Esta
especial orientaci6n es debida a la presencia de numerosos granulos de
almid6n en las celulas del cotiled6n. Tal orientaci6n dirige la plumula
hacia arriba en la germinaci6n y al mismo tiempo numerosos pelos de
raiz se forman en la parte inferior del lado del cotiled6n, para fijar la
planta joven en la arena inestable del fondo.
LITERATURE CITED
A.
1920. Water plants-a
study of aquatic angiosperms. Cambridge University Press, 436 pp.
ARBER,
ASCHERSON, P., AND M. GURKE
1889. Hydrocharitaceae.
2(1): 238-258.
In
Engler
and
Prantl.
Natur.
Pflanzenfam.
BALFOUR, B.
1878. On the genus Halophila. Trans. bot. Soc. Edinb. 13: 290-343.
N. L. AND C. F. MILLSPAUGH
1920. The Bahama Flora. Pub\. by the authors, N. Y.
GRISEBACH, A. H. R.
1864. Flora of the British West Indian Islands. Lowell Reeve and Co.,
London.
HUMM, H. J.
1956. Seagrasses of the northern Gulf coast. Bull. Mar. Sci. Gulf & Carib.
6: 305-308.
LAWRENCE, G. H. M.
1951. Taxonomy of vascular plants. MacMillan and Co., New York,
xiii + 823 pp.
MOORE, D. R.
1963. Distribution of the sea grass, Thalassia, in the United States. Bull.
Mar. Sci. Gulf & Carib., 13: 329-342.
MUENSCHER, W. C.
1944. Aquatic plants of the United States. Comstock Publ. Co., Ithaca,
N. Y., 374 pp.
PHILLIPS, R. C.
1960. Observations on the ecology and distribution of the Florida seagrasses. Fla. State Bd. Conserv. Mar. Lab., Professional Pap. Ser.,
No.2: 1-72.
RYDBERG, P. A.
1909. The flowers and fruits of the turtle-grass (Thalassia). J. N. Y. bot.
Odn., 10: 261-265.
SMALL, J. K.
1903. Flora of the southeastern United States, Pub\. by the author, N. Y.,
through New Era Printing Co., Lancaster, Penna. 1394 pp.
1933. Manual of southeastern flora. Publ. by the author, N. Y., through
Sdence Press Printing Co., Lancaster, Penna. 1554 pp.
THORNE, R. F.
1954. Flowering plants of the waters and shores of the Gulf of Mexico.
Fish. Bull., U. S., No. 89, 55: 193-202.
Voss, G. L. AND N. A. VOSS
1955. An ecological survey of Soldier Key, Biscayne Bay, Florida. Bull.
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BRITTON,·