Hydrophilous Pollination of a Dioecious Seagrass ...

Hydrophilous Pollination of a Dioecious Seagrass, Thalassodendron ciliatum (Cymodoceaceae) in
Kenya
Author(s): Paul Alan Cox
Source: Biotropica, Vol. 23, No. 2 (Jun., 1991), pp. 159-165
Published by: The Association for Tropical Biology and Conservation
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BIOTROPICA 23(2): 159-165 1991
Hydrophilous Pollination of a Dioecious Seagrass,
Thalassodendron ciliatum (Cymodoceaceae) in Kenya'
Paul Alan Cox
Department of Botany and Range Science, Brigham Young University, Provo, Utah 84602 U.S.A.
ABSTRACT
The flowering of the dioecious seagrass Thalassodendron ciliatum (Cymodoceaceae) in Kenya is coincident with
extremely low spring tides. Staminate plants release their flowers underwater immediately before the low tide begins
to return. These float to the surface and there they expel the filamentous pollen. The pollen form floating snowflakelike
rafts (search vehicles) that collide on the water surface with the female stigmas. Since pollination occurs on the
water surface, T. ciliatum has a category 2 hydrophilous pollination system, strikingly similar to that of Amphibolis.
Seeds of the developing fruit germinate precociously and seedling development is viviparous.
UFUPISHO
Mikuku ni niti yenye maua ambayo ina mea kwenye maji madago ya bahori kwenye mwambo wa kenya. Ina zoa
maua katika mwezi wa kuna miti tofauti ya kiume na ya kike. Maji ya kifuma, maua ya kiume huwa ya kiogelea
juu juu ya maji ya bahari. Mbelewe (pollen) ya maua ya kiume huwa ikiondoka na kvogelea kwenda kwenye maua
ya kike. Baadaye mimea michanga inaanza kumea kwenye mimea ya kike na baadye huwa ikiachiliwa.
WITHIN THE LAST DECADE, there has been a renewed theoretical predictions; thus a series of investigations
interest in abiotic pollination systems, induding hy- on the pollination biology of seagrasses has been
drophilous pollination. As defined by Delpino and initiated (Cox 1988, 1990; Cox, Laushman, &
Ascherson (1871), Knuth (1898), Ernst-Schwar- Ruckelshaus 1990; Cox, Elmqvist, & Tomlinson
zenbach (1944), and Cox (1988), hydrophilous 1990; Cox & Knox 1988,- 1989; Cox & Tomlinson
pollination involves water as a vector for the trans- 1988).
portation of pollen, or the transportation of con- The seagrass genus Thalassodendron den Hartog
veyances (such as the flowers of Vallisneria) that (Cymodoceaceae) has two species: T. pachyrhizum,
carry the pollen. For ease of discussion, hydrophilous which is confined to limestone reef platforms on the
pollination systems can be divided into three eco- western coast of Australia (den Hartog 1970, Kirklogical
dasses: Category 1, in which pollen is trans- man & Cook 1987); and T. ciliatum (Forsk.) den
ported above the water surface; Category 2, in which Hartog, which ranges from East Africa (W. Isaac
pollen is transported on the water surface, and Cat- 1968, F. Isaac 1968) through the Indian Ocean to
egory 3, in which pollen is transported beneath the Indonesia (Brouns 1985), Papua New Guinea
water surface (Ernst-Schwarzenbach 1944, Cox (Johnstone 1984), the Solomon Islands (Johnstone
1988). The use of a search theory and dassical 1982), and the northwest coast of Australia (Walker
diffusion mechanics has prompted a reexamination and Prince 1987). The taxonomy of the genus toof
hydrophilous pollination systems, since two-di- gether with notes on the structure of the floral units
mensional pollination systems with pollen dispersed has been described by den Hartog (1970). The floral
in large aggregations or conveyances have been pre- morphology of T. ciliatum has been described by
dicted to be advantageous (Cox 1983). Basic field Isaac (1969) and Kay (1971), pollen development
observations of the pollination ecology of many hy- by Ducker et al. (1978) and Pettitt (1981), vegdrophilous
plants however are lacking (Cox 1988). etative morphology by Tomlinson (1982), and fo-
Reliable information on the pollination of seagrasses liar anatomy by Barnabas (1982). The floral morhas
been particularly needed in order to test these phology of T. pachyrhizum has been described in
some detail by Kuo and Kirkman (1987). No pre-
I Received 12 October 1989, revision accepted 23 April vious observations have been reported on the pol-
1990.
lination mechanism of either species of Thalasso-
159

160 Cox
dendron although Isaac (1969) reported finding an the horizontal shoot becomes erect. The erect portion
anther of T. ciliatum in a tide pool with pollen of the shoot is distinctly dorsiventral, being elliptical
strings extruded from it.
in cross section, and produces foliage rather than
Thalassodendron ciliatum is called "Mikuku" scale leaves. Older erect shoots may branch, infrein
Swahili and is well known to villagers of the quently producing at their base a new horizontal
Watamu area, who readily distinguish it from En- shoot with scale leaves; or, as is more common, they
halus acoroides, which is used as a famine food. produce an erect shoot higher up. If the apex of the
original erect shoot is damaged, an axillary bud
beneath the shoot apex may produce a renewal
METHODS
shoot. Erect shoots have a maximum of three orders
of branching. The erect shoots (Fig. 1A) are disti-
A population of Thalassodendron ciliatum was studchous
with alternate leaves, with the flowers of pisied
at Watamu Bay on the east coast of Kenya
tillate plants being borne on short lateral shoots in
during extremely low spring tides from 20 to 25
the axils of leaves near the shoot apices. Thalasso-
October 1988. Several large rhizome systems were
dendron appears to be dioecious, as all of the rhizome
unearthed and studied. Twenty male and twenty
systems I unearthed were completely unisexual.
female erect shoots were collected and the number
The flowers are borne on short lateral branches
and distribution of flowers on each shoot were reproduced
in the axils of foliage leaves near the apex
corded. Male and female floral units in differing
of erect shoots. The short lateral shoots bearing the
stages of maturity were collected and preserved in
pistillate flowers are two nodes long before pro-
FAA, critical point dried and sputter coated with a
ducing the first of four specialized auriculate floral
gold amalgam in preparation for study by scanning
bracts enclosing the axis, with the axis terminating
electron microscopy.
in a floral unit with two carpels. This unit may be
The pollination biology of T. ciliatum was studtermed
a "flower," but see Tomlinson (1982) for
ied in the field using snorkel gear. The population
a discussion of the comparative morphology of such
was observed before, during, and after low spring
structures in the Helobiae. Each carpel (Fig. 1C),
tides for release of male floral units. The diameters
which is 2 mm long, contains a single ovule, and
of floating pollen search vehicles were measured.
terminates with a style 3-5 mm long, bifurcating
The orientations of the stigmas of the female plants
into two filiform stigmas, each being approximately
were observed and photographed at low tide.
5.0 cm in length. At maturity, these stigmas pro-
Voucher specimens of both male (Cox 1400, 1405)
trude through the bracts and in intertidal plants are
and female (Cox 1401) plants were made and are
exposed to the water surface at extremely low tides
on deposit at the Brigham Young University Her-
(Fig. 1B). The portions of stigmas exposed outside
barium (BRY) and the Gray Herbarium (GH) of
of the bracts, however, soon break off subsequent
Harvard University.
to pollination or as the result of damage (Fig. 1D).
The stigmatic surface is smooth, with no papillae
or other structures visible (Fig. 2D).
RESULTS
The short shoots bearing the staminate flowers
At Watamu Bay, Kenya, Thalassodendron ciliatum are also borne in the axils of foliage leaves, and at
occurs in small depressions in the raised coral plat- the first node produce the first of four floral bracts,
form, as large patches in the subtidal, and at the the inner three being distinctly auriculate. The stamouth
of Mida Creek, which is a nearby estuary. minate floral unit (hereafter termed "flower") is 1.5
The distichous axes of T. ciliatum begin as plagi- cm long, and produces two fused anthers each with
otropic axes, but become orthotropic at the fourth four locules. Inside each locule, the long filamentous
internode, producing the aerial axis. Continuation pollen is tighdy coiled (Fig. 2A). The anthers deof
the rhizome system is by development of a shoot hisce by means of longitudinal slits (Fig. 2B), reproduced
from the bud in the axil of the scale leaf leasing the filamentous pollen.
at the fourth internode. The architecture of the Staminate shoots produce a median of eight
rhizome system is therefore sympodial, with the flowers per shoot while pistillate shoots produce a
precision of the change of the horizontal axis from median of two flowers per shoot. These medians
a horizontal to an erect position at the fourth node are significantly different (sign test, P < 0.001).
being most striking. Development of the erect shoots During the week of 20 October, staminate flowbecomes
more pronounced in order of their age. ers were found attached to the staminate plants but
Roots are produced only at the fourth node where they did not abscise in mass until the low spring

;~~~~~~~~~~
Hydrophilous Pollination 161
FIGURE 1. Thalassodendron ciliatum in Watamu, Kenya. A. Erect shoots with foliage leaves. B. Pistillate plant
at low tide with filiform stigmas protruding from bracts and exposed to water surface. C. Pistillate floral unit with
bracts removed, showing the two carpels each with two filiform stigmas. Grid size = 1 cm. D. Pistillate floral unit,
with the ovary pictured in the front unpollinated, and the other ovule fertilized with the viviparous seedling attached.
Grid size = 1 cm.

162 Cox
@+.~~~~~~~~~~~~ -*d.
4f ~ ~ ~ ~ t~
FIGURE 2. Thalassodendron ciliatum, details of staminate floral unit. A. Anther with tip broken off exposing
tightly coiled filamentous pollen. Scale bar = 100 gm. B. Anther dehiscing by longitudinal slit. Scale bar = 1 mm.
C. Filamentous pollen. Scale bar = 100 ,um. D. Thalassodendron ciliatum stigma section. Scale bar = 100 gm.
tides of 24 and 25 October which were the lowest reaching the surface, the anthers dehisce and expel
tides in the tidal cyde (Figs. 3, 4A). As the tide the filamentous pollen, and are washed up in mass
returned, the surface of the water was filled with on the beach as the tide returns (Fig. 4C). The
the small floating staminate flowers (Fig. 4B). On filamentous pollen grains, when released in this fashion,
float and form snowflake-like search vehides
(Fig. 4D) of median diameter 0.95 cm. The ad-
Daily Tidal Fluctuations, Kenya
5
herence of the individual pollen "noodles" into search
vehides may be mediated by the coating on the
4
pollen wall formed by the periplasmodial residue
as described by Pettitt (1981). These search vehides
3
are not significantly different in size (Mann-Whitmey
Z = 1.145, P < 0.126) from the search vehides
E
la2
of Amphibolis antarctica in the related genus Amphibolis
(Fig. 5) as determined by data previously
gathered by Cox and Knox (1988). As the tide
returned, some of the search vehides collided with
0
Thalassodendron
r ase
r
the stigmas exposed at the surface of the water (Fig.
1B), thereby effectng pollination. Thalassodendron
5 10 15 20 25 30 5 ciliatum therefore has a type 2 hydrophilous pol-
October November
lination system following the categories proposed
FIGURE 3. Tidal cyde for Watamu, Kenya from 1 by Cox (1988).
Oct. to 5 Nov. 1989. Mass release of Thalassodendron After pollination, development of the seedling
ciliatum staminate flowers coincided with the lowest spring is viviparous (Fig. 1D) with usually only one of the
tides on 25 and 26 Oct.
pair of carpels developing into a fruit.

T 8 - I -J
g 'Ut
_
Hydrophilous Pollination 163
FIGURE 4. Thalassodendron ciliatum A. T. ciliatum population at Watamnu, Kenya exposed by extremely low
spring tide, 26 Oct. 1988. B. Staminate floral unit floating on water surface at low tide prior to dehiscence. C.
Staminate floral unit after dehiscence and pollen release. Grid size = 1 cm. D. Pollen rafts or search vehides of
Thalassodendron ciliatum pollen floating on water surface at low tide. Grid size = 1 cm.
^~~~~~~~~~~~~~~~~~~~~~~z

164 Cox
Search Vehicle Size Distribution
._C
ThalassodendronW
5 10 15 20 25 30
Diameter (mm)
FIGURE 5. Size distribution of pollen rafts or search vehides for two surface-polinated seagrasses, Thalassodendron
ciliatum at Watamu, Kenya and Amphibolis antarctica at Point Lonsdale, Australia.
DISCUSSION
the nearly synchronous underwater abscission of staminate
flowers that float to the surface, dehisce, and
In both Kenya and northwestern Australia, Thalasrelease
their pollen forming floating search vehides
sodendron ciliatum has been described as being found
has been previously reported only for Amphibolis
in intertidal pools on "raised reef areas where it is
antarctica in Australia (Cox and Knox 1988, Ducknever
emersed" (W. Isaac 1968, Walker & Prince
er et al. 1978, fig. 15). The similarities in surface
1987). However, F. Isaac in Kenya reported "In
pollination mechanisms between Amphibolis antthe
intertidal area it is never fully exposed although
arctica and Thalassodendron ciliatum are most strikat
low water spring tides the leaves can be seen at
ing, induding viviparous development of the seedthe
surface. If the water is very low the flexible
ling, and suggest dose phylogenetic affinities.
stems fall sideways to remain in the water" (F. Isaac
Submarine pollination in either species cannot be
1969, p. 46). It is precisely at these extreme low
exduded on the basis of field studies conducted to
tides, when the tops of Thalassodendron plants lie
date; information regarding the pollination biology
on the surface of the water, that surface pollination
of Thalassodendron pachyrhizum, whidc has yet to
occurs. Although when uncovered by the low spring
be found in as shallow water as T. ciliatum (Kirktide,
the leaf tips of T. ciliatum show signs of
man and Cook 1987, Walker and Prince 1987),
desiccation, the plants seemed to exhibit no ill efwould
be most interesting.
fects. It is interesting in this regard that McMillan
(1984) found, in contrast to many other genera of
seagrasses, that T. ciliatum plants from Kenya were ACKNOWLEDGMENTS
able to withstand high temperature sea water (390C)
I thank Mohammed Alale and James Charo for their
for 36 hours. He found that even though the leaves assistance in data collection and their patience in helping
and apical buds were lost, new leaves were initiated me with Swahili, the Keeper of the Herbarium, British
at the bases of the stems.
Museum (Natural History) and the Director of the Her-
Tidally synchronized rhythms of flowering in barium of the University of Uppsala for access to their
collections, and P. B. Tomlinson for useful discussions.
seagrasses are a common phenomenon (Pettitt 1984),
This study was supported by a National Science Founand
have been studied in Kenya (in Thalassia hem- dation Presidential Young Investigator Award BSRprichii)
in some detail by Pettirt (1980). However, 8452090.
CD

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