J. Phycol. 42, 43–50 (2006)
r 2005 Phycological Society of America
DOI: 10.1111/j.1529-8817.2006.00184.x
ONTOGENETIC CHANGES IN BUOYANCY, BREAKING STRENGTH, EXTENSIBILITY,
AND REPRODUCTIVE INVESTMENT IN A DRIFTING MACROALGA TURBINARIA
ORNATA (PHAEOPHYTA)1
Hannah Louise Stewart2,3
Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA
Turbinaria ornata (Turner) J. Agardh is a tropical
alga that disperses by detached, reproductively mature floating fronds. Material properties (breaking
stress, breaking extension), buoyancy, and the proportion of reproductive tissue per frond were measured for juvenile, adult, and old fronds of T. ornata.
Correlations between these factors indicate that as
fronds age and become more reproductively mature, the tissue in their stipes (where they break)
becomes weaker, more brittle, and the overall buoyancy of the frond increases. Measurement of drag
force experienced by fronds from each ontogenetic
stage allowed calculation of the environmental
stress factor (ESF), which indicates the likelihood
of detachment of a frond in the flow environment of
its habitat. The ESF for fronds of each ontogenetic
stage predicted that reproductively mature fronds
(adult and old) break more readily than immature
(juvenile) fronds. Increased proportions of reproductively mature fronds in floating rafts following
storms compared with the proportion of mature
fronds attached to the substratum support the ESF
predictions. This combination of ontogenetic
changes in material properties, buoyancy, and reproductive maturity in combination with the life
history of T. ornata may contribute to the dispersal
of this alga throughout French Polynesia.
storms (Tunnicliffe 1981, Highsmith 1985, Bruno
1998, Boller et al. 2002), while some erect branching
sponges propagate almost exclusively by asexual fragmentation (Wulff 1991). Colonies of adult ascidians
have weak attachment to the surfaces, and therefore
are often dislodged from the substratum, and can reattach in new areas (Worcester 1994, Edlund and
Koehl 1998). Many species of marine macroalgae
(Pearlmutter and Vadas 1978, Santelices and Doty
1989, Ceccherelli and Cinelli 1999, Smith and Walters
1999) and sea grass (Cambridge et al. 1983, Kuo and
Kirkman 1987, Ewanchuk and Williams 1996) can also
reattach after dislodgement or fragmentation, resulting in asexual dispersal.
In addition to asexual propagation, drifting can also
facilitate long-distance dispersal of propagules released
by organisms as they drift and/or upon arrival to suitable substratum (Norton 1992). This can greatly increase the distances propagules disperse, as detached
organisms that remain at the surface or in the water
column can move great distances on wind and ocean
currents. Dispersal distances of algal gametes, spores,
and some larvae range from a few centimeters to a few
meters (Dayton 1973, Paine 1979), but may reach up
to several kilometers depending on currents (Reed
et al. 1992, Todd et al. 1998, Gaylord et al. 2002,
Shanks et al. 2003). However, rafts of buoyant seaweeds have been reported to float at the surface for up
to 6 months (Helmuth et al. 1994), and can cover distances up to thousands of kilometers. For example,
several species of buoyant brown algae were found to
have drifted 1000 km from New Zealand to the
Kermadec Islands (Nelson and Adams 1984). Durvillaea antarctica from west coast Australia has been found
5000 km from the nearest source (Kenneally 1972).
French and British populations of Sargassum muticum
are thought to be point sources for drift fronds found
in the Dutch delta region (Critchley et al. 1987). Thus,
the combination of drifting and propagule release can
greatly increase the distance over which dispersal of
sessile organisms can occur, relative to propagule
dispersal from a sedentary organism.
Whether a fragment or whole organism detaches
from the substratum depends on the strength of its
attachment relative to the force acting to dislodge or
break it. Breaking strength, or the force required to
break a structure divided by its cross-sectional area, is a
function of a structure’s material properties and shape.
Key index words: buoyancy; environmental stress
factor; macroalga; material properties; morphology; ontogeny; Turbinaria ornata
Abbreviations: ESF, environmental stress factor
In the marine environment, the movement of detached whole or large pieces of sessile organisms by
water motion is a common dispersal mechanism. For
example, the dominant form of propagation in some
reef-building corals and gorgonians is through reattachment of colony fragments broken off during
1
Received 3 February 2005. Accepted 1 October 2005.
Author for correspondence: e-mail [email protected].
3
Present address: Marine Science Institute, University of California, Santa Barbara, CA 93106-6150, USA.
2
43
44
HANNAH LOUISE STEWART
Hydrodynamic forces exerted on sessile organisms in
moving water are also dependent on the morphology
of the organism (Denny 1988). As both breaking
strength and hydrodynamic force are functions of
the size and shape of an organism, ontogenetic changes in morphology can affect the potential for detachment of sessile organisms as they grow. The probability
of dispersing via this mechanism may then change
throughout the lifetime of the organism. Calculation of
the likelihood of detachment given the morphological
and biomechanical properties of the organism at a particular ontogenetic stage and the flow it encounters in
its habitat at that stage (the ‘‘environmental stress factor (ESF)’’ (Johnson and Koehl 1994) enables predictions of detachment relevant to the life history and
environment of the organism.
Turbinaria ornata (Division Phaeophyta, Order Fucales) is a perennial macroalga common throughout
volcanic islands in the South Pacific Ocean. It differs
morphologically between high-flow and low-flow sites
(Payri 1984, Stewart 2004). Fronds from forereef sites
that experience wave-driven flow are shorter and have
different morphological and material properties than
fronds from calm backreef habitats dominated by relatively calm, unidirectional flow (Stewart 2004). Buoyancy is a plastic trait in response to water motion in
T. ornata, with non-buoyant fronds becoming buoyant
after transplantation to calm areas (H. L. Stewart,
in press).
Dispersal in T. ornata can operate over two spatial
scales; long distance dispersal of detached buoyant
fronds that drift on surface currents and small-scale
dispersal of germlings released from parent fronds.
Buoyant fertile floating fronds of T. ornata that detach
from the substratum can form rafts that may contain
thousands of thalli (C. E. Payri, personal communication) and may travel hundreds of kilometers on surface
currents (Stiger and Payri 1999a, b, 2005). The abundance and distribution of T. ornata throughout French
Polynesia has increased significantly since the 1980s
(Payri and Stiger 2001, Stiger and Payri 2005), and
dispersal by rafting of T. ornata may contribute to its
success in this region (Stiger and Payri 1999a, b, Payri
and Stiger 2001).
To examine whether ontogenetic changes in T. ornata contribute to its potential for detachment and
drifting, the properties and hydrodynamic force that
contribute to the probability of detachment of T. ornata,
and changes in buoyancy and reproductive maturity
that contribute to the potential for rafting and fertilization success were examined to address the following
questions: (1) What are the ontogenetic changes in
buoyancy and reproductive investment in T. ornata? (2)
How do stipe material properties and hydrodynamic
force experienced by fronds of T. ornata change with
ontogeny? (3) What is the predicted potential for detachment and floating of fronds at different ontogenetic stages?, and (4) How do those predictions
compare with ontogenetic stages of fronds found floating on rafts in nature?
MATERIALS AND METHODS
Categorizing ontogenetic stages. The morphology of T. ornata
varies between forereef and backreef habitats (Payri 1984,
Stewart 2004). Therefore, fronds of T. ornata used in this experiment were all collected in September and October 2002
from the backreef of the barrier reef (S 171 28.699 0 W 1491
50.215 0 ) to the west of Cook’s Bay, between Tareu and Taotai
passes on the island of Moorea, French Polynesia. Fronds
were collected randomly from coral bommies along 30 m
transects in the backreef that paralleled the reef crest. Fronds
were returned immediately to the lab and held in shaded
seawater tanks. Buoyancy, material properties, and reproductive investment of fronds were all quantified within 1 day
of collection.
To make comparisons between fronds at different ontogenetic stages, fronds of T. ornata were classified into ontogenetic
groupings of juvenile, adult, and old. ‘‘Juveniles’’ were categorized as all fronds that did not yet have any reproductive receptacles. Fronds with reproductive receptacles and few
epiphytes were classified as ‘‘adults’’ (Stiger and Payri 2005a).
Reproductive fronds with over 50% of their surfaces covered
with epibionts were considered ‘‘old.’’ This categorization follows similar distinctions for old fronds as was used by Brown
et al. (1997).
Ontogenetic changes in buoyancy and reproductive investment. Eight fronds of each ontogenetic stage were collected
for determination of ontogenetic changes in buoyancy and
reproductive investment.
Net buoyant force (FB) on each algal frond was determined
using the following equation:
FB ¼ gVðra rw Þ
ð1Þ
2
where g is the acceleration due to gravity (9.81 m/s ), V is the
volume of the alga, ra is the density of the alga, and rw is the
density of seawater (1023 kg/m3 at 251 C; Vogel 1994). The
volume of each frond was determined to the nearest cm3 by
measuring displacement of water in a graduated cylinder after
a whole frond had been submerged. Fronds were then blotted
dry with paper towels and the mass of each frond was determined from the mean of two measurements. Dividing the mass
of each frond by its volume yielded estimates of the density of
each algal frond.
Reproductive investment was measured as described by
Arenas and Fernandez (1998). Reproductive tissue of T. ornata
is restricted to receptacles that are easily distinguishable from
vegetative tissue. Fronds were quickly rinsed with fresh water
to prevent salt crystals from seawater from being included in
the mass measurements. All reproductive tissues were cut-off
the frond, and both reproductive and vegetative tissues were
dried at 601 C for at least 48 h or until its mass stopped changing in consecutive weighing. The mass of each frond and of its
reproductive tissue was determined from the mean of two
measurements to the nearest 0.01 g. The reproductive investment of each frond was determined by dividing the dry mass
of all receptacles by the total dry frond mass (including
receptacles).
Material properties. To determine whether tissue material
properties of T. ornata change with ontogeny, extension ratio
and breaking stress of T. ornata stipes were measured by conducting tensile stress-extension tests on T. ornata stipes (as
described by Koehl and Wainwright, 1977) using a tensometer constructed for field use. Measurements were made for
eight fronds of each ontogenetic stage. The stipes of T. ornata
were used for these tests, as this was where fronds broke
when pulled experimentally from the substratum, and
fronds found in floating mats were all broken along the stipe.
One end of each stipe was clamped onto a stationary, machined aluminum beam. The other end of the stipe was
ONTOGENETIC CHANGE IN ALGAL MORPHOLOGY
clamped securely to a beam whose distance from the other
beam could be altered by a hand-cranked lead screw. The
original length of the portion of the stipe between the clamps
was measured to the nearest 0.1 mm with digital calipers.
The length of the stipe as it was pulled was measured using a
linear variable differential transformer (LVDT) (Pickering &
Co. Model 7308-X2-AO, Marietta, OH, USA) to the nearest
0.1 mm. The rate of extension was held constant by making
one rotation of the lead screw crank each second. This produced an extension rate of 0.016/s. Voltages from the LVDT
were recorded at 10 Hz and converted to digital signals using
a data acquisition card (National Instruments DAQ 1200,
Austin, TX, USA) and recorded on Labview software (National Instruments, Version 3.0). Voltage changes were transformed to length measurements using calibration equations
established by measuring the change in voltage for a known
increase in length (r2 5 0.95).
The extension ratio (l) is a measure of the extension of a
material, and was calculated using the following equation:
l ¼ ðL Lo Þ=Lo ;
ð2Þ
where Lo is the original length of the stipe being tested and L is
the length of the stipe as it was pulled.
The force with which the stipe resisted being extended was
measured by the strain gauges on the beam. Voltages generated from the deformation of the strain gauges as the stipe was
pulled in tension were passed through the bridge amplifier as
above. The force transducer was calibrated by hanging weights
from the beam by a string to the beam at the same location as
the algal stipes had been attached. The string was laid over a
pulley attached to the edge of the table so that the mass of the
weight caused a horizontal displacement of the beam, as occurred when the algal stipes were pulled. Weights of known
masses were hung from the transducer. Each weight was hung
three times and the mean of the voltages registered for each
weight was multiplied by the acceleration due to gravity
(9.81 m/s2) to yield the force applied to the beam. A linear regression (r2 5 0.86) was calculated for the relationship between
voltage and force, with a precision of 0.001 N.
The breaking stress (sBRK) is the stress at which the specimen broke and is a measure of the strength of the tissue. The
breaking stress (s) for each stipe as it was pulled was calculated
by
s ¼ F=A;
ð3Þ
where F is the force required to break the specimen and A is
the cross-sectional area of the stipe at the point at which it
broke. The diameter of each stipe was measured using callipers
with a precision of 0.1 mm, and the area calculated using the
equation for the area of a circle, as stipes were roughly circular
in cross section.
Predicting the potential for detachment—drag force and
ESF. The potential for detachment of a frond depends on
the force it experiences in moving water and its ability to
contend with that force. Because backreef fronds of T. ornata
are exposed primarily to unidirectional water flow, drag
force is the predominant hydrodynamic force acting on
fronds as they are pulled in tension by water moving around
them. Calculation of the drag force and the material properties of the stipe (measured above) allowed estimation of the
ESF, a measure of the likelihood of detachment of fronds in
the backreef.
Drag. It was not possible to measure drag on the same
individuals that were used in the material properties experiments, because in those experiments fronds were used immediately upon collection and broken in the course of
measuring their breaking strength and extensions. Therefore, the drag force that these fronds likely would have ex-
45
perienced at a range of unidirectional flow velocities was
estimated as follows.
Drag force (Fd) on macroscopic objects in moving water is
given by
Fd ¼ 12rU2 SCd
ð4Þ
where r is the density of water, U is the velocity of the water
past the body, S is the plan area of the object, and Cd is the drag
coefficient, a function of the shape of the object. As S and Cd
are properties of the individual fronds, these parameters were
estimated for backreef fronds of the same length as those used
in the material properties experiments.
The planar area (S) of fronds of the lengths used in the
material properties experiment was approximated from a correlation established between length and planar area (r2 5 0.65)
of 10 randomly collected backreef fronds. Both parameters
were determined from the mean of two measurements of digital photos using NIH image software (version 1.61, National
Institute of Health, Bethesda, MD, USA).
Drag measurements were conducted in a flow tank at the
University of California at Berkeley using fronds that had been
transported from Moorea. Fronds were collected wrapped in
wet paper towel and enclosed in an airtight plastic bag for 12 h
during air transport from Moorea to Berkeley, where they
were held in an aerated saltwater aquarium. Fronds were used
in the drag experiments up to 3 days after collection, and
damage or disintegration of tissue was not evident at that time.
Drag measurements were conducted in a flow tank with a
working section of 0.35 0.50 2.00 m. Water velocity in the
tank was measured at average mid-frond height of adults
(8.0 cm) with an acoustic Doppler anemometer (SonTek Inc.,
San Diego, CA, USA) to the nearest 0.001 m/s. Drag on each
frond was measured with force transducers (Koehl 1977).
Fronds were attached at the base of their stipes with a cable
tied to the sting of a force transducer that poked up through a
false bottom on the floor of the flow tank. The force signal was
passed from the transducer through the bridge amplifier to
the DAQ card recorded on Biobench software (National Instruments, Austin, TX, USA) on a laptop computer. Voltages
from the force transducer were recorded at 10 Hz and averaged over 30 s intervals.
The force transducer used in the drag experiments was
calibrated in the same manner as that used in the material
properties tests described above. A linear regression (r2 5 0.88)
was calculated to describe the relationship between voltage and
force, with a precision of 0.001 N.
The drag coefficient (Cd) was estimated to be the mean of
the drag coefficients measured for ten adult backreef fronds at
a range of flow speeds from 0.16 to 0.73 cm/s in a unidirectional flow tank. The drag force that would likely have been
experienced by the fronds of the lengths used in the material
properties tests was then calculated using the Cd and the S estimated as above. As the Cd did not change significantly between flow speeds, the Cd at the highest flow speed (0.73 m/s)
was used in drag calculations to extrapolate to drag forces at
flow speeds faster than those possible in the flume. This may
have overestimated drag at higher flow speeds as Cd can decrease as flow speeds decrease (Carrington 1990). Drag was
estimated at flow speeds from 0.73–3.5 m/s, a range of flow
speeds that spans estimates of instantaneous maximum flow
speed in the backreef (1.0–1.25 m/s J. Hench, personal communication).
The mean values of drag of the 10 measurements for each
ontogenetic stage at the highest flow speed in the flume
(0.73 m/s) were compared using a one-way ANOVA and a
Tukey–Kramer multiple comparison in Matlab (version 7.01,
Mathworks Inc., Natick, MA, USA).
ESF. The ESF is a measure of the resistance to detachment or breakage of an organism at a particular time in its
46
HANNAH LOUISE STEWART
beginning with 12:00 p.m. in the North direction. All transects passed through the center of the raft. A total of 179
fronds were collected from four rafts.
Ontogenetic stage and length of attached fronds were determined by collecting all fronds within 10 cm on one side of
three 10 m transect tapes placed randomly within the backreef.
The ontogenetic stage was determined as above. A total of 214
fronds were collected from the three transects.
0.3
0.25
0.08
0.06
0.15
0.1
0.05
0.04
0.02
0
–0.02
0
r 2=0.81 p<0.05
0
5
10
15 20 25
Length (cm)
30
35
10
8
6
4
2
r 2=0.48
0
0
5
10
15 20 25
Length (cm)
r 2=0.78 p<0.05
– 0.04
D
1.5
Breaking extension ratio
Breaking stress (MN . m–2)
B
0.2
–0.05
C
RESULTS
Ontogenetic changes in buoyancy and reproductive
investment. Net buoyant force of fronds of T. ornata
increased with frond length and advanced ontogenetic stage (Figs. 1 and 2). This appears to be due to
the increased relative volume of pneumatocysts inside blades at the distal portion of fronds relative to
blades proximal to the holdfast. The reproductive
receptacles of T. ornata are independent ancillary
structures (Fig. 3), and the proportion of frond dry
mass made up of reproductive tissue increased with
frond length and with advanced ontogenetic stage
(Fig. 1). Reproductive tissue made up 20% of total
biomass in adult fronds and up to 25% in old fronds
(Fig. 2). Net buoyant force experienced by fronds of
T. ornata increased with proportion of mass made up
of reproductive tissue (Fig. 2).
Net buoyant force (N)
A
Proportion mass reproductive
ontogeny, relative to the peak forces it experiences in its
habitat at that time (Johnson and Koehl 1994). The ESF is
calculated from the ratio of the breaking stress of the stipe at
a particular stage in its ontogeny (calculated above) divided
by the stress owing to drag experienced by the frond in flow
velocities experienced during that season in its habitat.
For backreef fronds of T. ornata, the ESF was calculated as
the ratio of the breaking stress of the stipe (calculated above)
divided by the estimated stress owing to drag experienced by
each frond. Stress in the stipe owing to drag was calculated by
dividing drag force by the cross-sectional area of the stipe of a
frond of a particular length used in the material properties
tests.
An estimate of the ESF was calculated for ten fronds of each
ontogenetic group (juvenile, adult, and old) for flow speeds
from 0.16 to 3.5 m/s. An ESF of greater than 1 suggests that the
organism will not detach from the substratum and an ESF of
less than 1 predicts that the organism will break.
Ontogenetic stages of fronds floating in mats and attached to the
substratum. To compare predictions of detachment of T. ornata based on the calculated ESFs for each ontogenetic stage
to what was found in the field, the ontogenetic stage and
length of fronds attached to the substratum and floating in
rafts in a backreef were determined. Detached, floating
fronds were collected using random transects through four
floating rafts of T. ornata. Transects were conducted by driving a small skiff slowly through a raft and collecting all fronds
within 1 m on one side of the boat. The orientation of transects through the raft was determined using a random
number table to select a starting position around the edge
of the raft. Numbers from 1 to 12 were assigned like a clock
1.4
0
35
10
15 20 25
Length (cm)
30
35
30
35
1.3
1.2
1.1
r 2=0.68 p<0.05
p<0.05
30
5
1
0
5
10
15 20 25
Length (cm)
FIG. 1. Correlations between length (cm) and frond characteristics for juvenile ( ), adult (&), and old (4) fronds. (A) Proportion of
total frond dry mass made up of reproductive material, plotted as a function of frond length. (B) Net buoyant force (N) of fronds plotted
as a function of length. (C) Breaking stress (N/m2) plotted as a function of length of stipes pulled in tension. (D) Breaking extension ratio
as a function of length of stipes pulled in tension.
ONTOGENETIC CHANGE IN ALGAL MORPHOLOGY
A
0.08
47
r 2=0.61 p<0.05
Net buoyant force (N)
0.06
0.04
0.02
0
–0.02
B
10
Breaking stress (MN . m–2)
–0.04
–0.05
8
Breaking extension ratio
0.05
0.1 0.15
0.2 0.25
Proportion mass reproductive
0.3
r 2=0.46 p<0.05
6
4
FIG. 3. Photograph of a blade of Turbinaria ornata with reproductive receptacle.
2
0
–0.05
C
0
0
1.5
0.05
0.1 0.15
0.2 0.25
Proportion mass reproductive
0.3
r 2=0.57 p<0.05
1.4
1.3
1.2
1.1
1
–0.05
0
0.05
0.1 0.15
0.2 0.25
Proportion mass reproductive
0.3
FIG. 2. (A) Net buoyant force (N). (B) Breaking stress (MN/
m2). (C) Breaking extension ratio, plotted as functions of the
proportion of mass made up of reproductive material for juvenile ( ), adult (&), and old (4) fronds.
Material properties. Breaking stress and breaking
extension ratio of stipes of T. ornata decreased with
frond length and advanced ontogenetic stage (Fig. 1),
and with reproductive investment (Fig. 2).
Potential for detachment—drag and ESF. Drag force
increased with flow velocity from 0.16 to 3.5 m/s and
was higher for old and adult fronds than juvenile
fronds at all flow speeds (Fig. 4). These values likely
overestimate drag at high flow speeds, as the value
for Cd at the highest flow speed possible in the flume
(73 cm/s) was used to calculate drag forces at flow
speeds faster than those possible in the flume. In
general, Cd for algae is expected to decrease with increasing flow speed as algae are reconfigured into
increasingly streamlined shapes as flow gets faster
(Carrington 1990). At the highest flow speeds generated by the flume used in this experiment, there was
no evidence of decreasing Cd, although it is likely that
Cd would have decreased at higher flow speed. However, the unique pinecone-like shape of T. ornata does
not streamline like other foliose algae, and so the extent to which the Cd may have decreased is difficult to
estimate. A decrease in the coefficient of drag would
tend to increase the ESF for all stages, but not likely
change the relative ESF of the different stages.
Calculations of the ESF for all ontogenetic stages
showed that ESF decreased with increasing flow speeds
from 0.16 to 3.5 m/s, and that ESF was higher for juveniles than for adults and old fronds (Fig. 4). Thus,
mature (adult and old) fronds should detach from the
substratum more readily than juvenile fronds.
Ontogenetic stage of fronds attached to the substratum
and floating in mats. Of fronds that were attached to
the substratum, 70% were juveniles, 26% were adults,
and 5% were old (Fig. 5). However, only one of the
179 fronds collected from the floating rafts was a juvenile, whereas 21% were adults and 79% were old
(Fig. 5).
48
A
HANNAH LOUISE STEWART
1
juvenile
adult
old
Drag (N)
0.8
0.6
0.4
0.2
0
0
0.1
0.2
0.3
0.4
0.5
Flow speed (m . s–1)
0.6
0.7
0.8
Environmental stress factor
B
100
juvenile
adult
old
10
1
0
1
2
3
4
5
0.1
Flow speed (m . s–1)
FIG. 4. (A) Drag force (N) measured at unidirectional flow
velocities from 0.16 to 0.73 m/s in a flow tank for juvenile ( ),
adult (&), and old (4) fronds (mean SE, n 5 10). Means at the
highest flow speed are significantly different from one another as
determined by a one-way ANOVA (f 5 163.52, df 5 2, Po0.05)
and Tukey–Kramer multiple comparisons. (B) Estimated mean
environmental stress factors (ESFs) at unidirectional flow velocities from 0.16 to 3.5 m/s for juvenile ( ), adult (&), and old (4)
fronds (mean SE, n 5 10). As the ESF approaches 1, the potential for breakage increases.
DISCUSSION
The correlations between increasing buoyancy and
reproductive maturity, and decreasing tissue strength
and extensibility with increasing ontogenetic stage noted in this study indicate a potentially important mechanism by which morphological ontogenetic changes
may contribute to the dispersal abilities of T. ornata.
The negative correlations between stipe breaking
strength and extensibility with ontogeny indicate that,
as fronds mature, their stipes become weaker and less
extensible. Older fronds are also longer and experience greater drag force than younger, shorter fronds.
Taken together, this increases the chance that older
A
B
juvenile
adult
old
FIG. 5. Proportion of juvenile, adult, and old fronds (A) attached to the substratum and (B) in floating rafts of Turbinaria
ornata in the backreef in Moorea in November 2003.
fronds, which are more reproductively mature and
buoyant, are more likely to detach as flow speeds increase, than are juveniles, as predicted by ESF. Indeed,
floating rafts of T. ornata are composed primarily of
mature fronds, with very few juveniles, supporting
predictions based on ESF. This is in striking contrast
to the proportions of juvenile, adult, and old fronds in
attached populations of T. ornata, in which juveniles
form the majority.
The positive correlation between reproductive capacity and buoyancy ensures that detached fertile floating fronds have the potential for sexual reproduction
in these mats. A survey of the ontogenetic stages of
fronds in mats in this study indicates that the vast majority (99%) of T. ornata fronds in mats are reproductively mature. Ova in female fronds are fertilized by
male gametes that are released in response to phases of
the moon (Stiger 1997), and fertilization success may
be enhanced for detached fronds that have been blown
together at the time of gamete release. Because release
of male gamete of T. ornata may take place in mats of
fronds, eggs from female fronds may be fertilized by
gamete from different male fronds, and it is conceivable that the population resulting from the zygotes of a
single female frond may be genetically diverse. Each
female frond of T. ornata can produce hundreds of
eggs, which only disperse up to 0.9 m from the parent
frond when released (Stiger and Payri 1999 b). In contrast to kelps, Fucales do not alternate sporophyte and
gametophyte generations. The gametophyte is reduced to eggs and sperm. Eggs are fertilized in and
retained within the receptacle of the female sporpphyte, and zygotes released from the female develop
directly into sporophyte fronds without intermediary
development of gametophyte fronds. They are therefore freed from the proximity and density settlement
requirements for female and male gametophytes that
can limit fertilization in kelps (North 1971). Therefore,
an individual fertilized female frond has the ability to
produce a genetically diverse population in a new area.
The life history of T. ornata combines aspects of
strategies that include fast-growing, short-lived weedy
species composed of weak thalli that produce spores
soon after settling and are easily broken by seasonal
storms, and strong, slow-growing space-holders that
are slow to produce spores and can grow back from
their holdfasts if broken off (Koehl 1984, 1999, Santelices and Varela 1994, Pratt and Johnson 2002).
Holdfasts of T. ornata are perennial, but thalli frequently break off from the holdfast during storms, leaving
the holdfast intact and attached to the substratum (H.
L. Stewart, unpublished data). Removal of the main
stipe of T. ornata results in the growth of one of the
small ‘‘ladies in waiting’’ fronds that are present in diminutive form at the base of the primary stipe on the
holdfast (H. L. Stewart and C. E. Payri, unpublished
data). Therefore, a stipe of a mature individual that is
detached from its holdfast is replaced by a frond of the
same genetic individual, while at the same time dispersing zygotes to new locations on reproductively
ONTOGENETIC CHANGE IN ALGAL MORPHOLOGY
mature fronds via rafting. This conveyor belt-like supply of reproductively mature fronds from individual
holdfasts likely contributes to the success of T. ornata.
The mean positive buoyant force experienced by
adult fronds (0.023 0.006 N) is small relative to hydrodynamic forces exerted on fronds in the backreef
on a relatively calm day ( 0.4 N) (Stewart 2004). However, this buoyant force contributes a tensile force to
the overall forces acting on the stipe. Perhaps more
importantly, the buoyancy of a detached frond maintains its position at the water’s surface, where it is subject to wind-driven surface currents. Currents and
wind congregate detached fronds from different locations into large mats, and fertilization in these mats
may help maintain genetic connectivity between populations, as mentioned above. Buoyancy also keeps detached fronds near the surface where light is abundant
for photosynthesis and may contribute to the long (3
month) period that T. ornata can stay alive and not disintegrate while floating (C. E. Payri, personal communication).
The factors affecting whether or not an alga will
detach from the substratum are varied (e.g. hydrodynamic regime, morphology, and ontogeny). Similarsized algae in the same habitat may have very different
ESFs, as was found for two intertidal seaweed species
Chondrus crispus and Mastocarpus stellatus, where differences in stipe cross-sectional area lead to different patterns of dislodgment in the same habitat (Dudgeon
and Johnson 1992, Pratt and Johnson 2002). The ESF
for an organism may also vary between season, site,
and life history stage. Changes to morphology that affect hydrodynamic forces and changes in tissue
strength can change the ESF an organism experiences. Such changes may occur in response to different
stages in an organism’s life cycle, as found in this study,
and in habitats experiencing different flow conditions
(Johnson and Koehl 1994, Pratt and Johnson 2002).
The combination of the life history of T. ornata, the
correlations between ontogenetic changes in material
properties, buoyancy, and reproductive investment is
well suited for the success of this species in the smattering of islands in the South Pacific. Islands range in
distance from one another from hundreds to thousands of kilometers, and floating mats of T. ornata may
drift between islands, establishing populations in new
locations and dispersing to adjacent islands (as suggested by Stiger and Payri (1999 b). Indeed the distribution and abundance of T. ornata throughout French
Polynesia has increased dramatically since the 1980s
(Payri and Stiger 2001, Stiger and Payri 2005) and
T. ornata is now common in areas where it had previously not been recorded.
SUMMARY
The results of this study indicate that during ontogeny, fronds of T. ornata experience an increase in the
proportion of tissue made up of reproductive tissue, an
increase in buoyancy, and a decrease in tissue breaking
49
strength and extensibility. Thus, as fronds age and
become reproductively mature, their stipes become
weaker and the buoyant forces they experience increase. In addition, fronds increase in size as they age,
increasing the hydrodynamic drag experienced by older algae in moving water. Thus older, fertile fronds face
increasing risk of detachment from the substratum,
and increased likelihood that detached fronds will
float. The ESFs of juvenile, adult, and old fronds indicate that the likelihood of detachment of adult or old
fronds (both of which are reproductively mature) is
greater than that of a juvenile at all flow speeds from 1
to 5 m/s. This prediction is supported by the pattern of
ontogenetic stages of fronds randomly collected from
four floating rafts of fronds in the backreef, the majority of which were fertile. These ontogenetic changes
to buoyancy, tissue strength, and reproductive capacity
in combination with the life history of T. ornata likely
play a role in the success of this alga.
Thanks to M. Koehl, T. Dawson, and M. Stacey for advice and
guidance throughout this project. Special thanks to C. Payri
for sharing her expertise on the natural history of T. ornata,
and to Ann Stewart, Jacques Yoo-Sing, and Tony Yoo-Sing for
help in the field. Comments from D. Reed and two anonymous reviewers improved the quality of this manuscript. This
research was funded by a graduate fellowship from the Natural Science and Engineering Research Council (NSERC) of
Canada, a PEARL graduate fellowship from the University of
California at Berkeley Richard R. Gump South Pacific Research Station, and a Ralph I. Smith Fellowship to H. L. Stewart. Additional funding was provided by National Science
Foundation grants #OCE9907120 and #OCE-0241447 to M.
Koehl and the Moorea Coral Reef LTER. This is contribution
#133 of UC Berkeley’s Richard B. Gump South Pacific
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