Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef
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- Stewart, H.L. Mar Biol (2006) 149: 721. doi:10.1007/s00227-005-0186-z
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Many aspects of morphology of benthic algae (length, surface area-to-volume ratio, and blade undulation) are plastic traits that vary in response to physical factors (such as light or water flow environment). This study examines whether frond buoyancy is a plastic trait, and whether differences in morphology including buoyancy affect the potential persistence of macroalgae in habitats characterized by different water flow regimes. Fronds of the tropical alga Turbinaria ornata in protected backreef environments in Moorea, French Polynesia possess pneumatocysts (gas-filled floats) and experience positive buoyant forces, whereas fronds in wave-exposed forereef sites either lack pneumatocysts entirely or have very small, rudimentary pneumatocysts and experience negative buoyant forces. Forereef fronds transplanted to the backreef developed pneumatocysts and experienced increased buoyant force indicating that buoyancy is a phenotypically plastic trait in T. ornata. In comparing the potential for dislodgement by drag, drag was greater on forereef fronds at low flow speeds as these fronds were stiffer and did not bend over at low flow speeds and therefore were less streamlined in the flow than backreef algae, which bent easily. The environmental stress factor (ESF) (a measure of the likelihood of detachment for a frond in its habitat) was higher for forereef than backreef fronds at all flow speeds. When examined with respect to the flow velocities likely in their respective habitats however, the chance of detachment for backreef and forereef was similar. Neither backreef nor forereef fronds were predicted to break under normal, non-storm conditions, but both were predicted to break in storms. Strong forereef morphologies are well suited to habitats characterized by rapid flow, whereas the weaker, buoyant, tall backreef fronds are well suited to habitats where crowding and shading is common but hydrodynamic forces are low.
Effects of frond morphology on hydrodynamic forces and danger of breaking
Water motion exerts hydrodynamic forces on benthic algae. The force experienced by an alga is a function of the interaction between its morphology and the flow it experiences in its habitat. This interaction can be affected by the alga’s size, shape, and the way in which it deforms in moving water (Carrington 1990; Koehl 2000). Large algae generally experience higher forces than small algae (Dudgeon and Johnson 1992), but many algae are reconfigured into streamlined shapes by water moving around them, reducing the drag force they experience (Koehl 1984, 1986; Carrington 1990). The extent to which an alga can be reconfigured depends on its shape and material properties: thin, flexible fronds can be streamlined more easily than stiff, bushy fronds. Flexible algae may also be pushed toward the substratum by moving water, and into slowly moving water lower in the benthic boundary layer, thereby reducing the velocity and the consequent hydrodynamic forces they experience.
Changes to morphology through development and ontogeny, and through phenotypically plastic responses to physical factors can change the forces algae experience in their habitats. The environmental stress factor (ESF, sensu Johnson and Koehl 1994) is a measure of the resistance to detachment of an organism at a particular time in its ontogeny, in its habitat. For algae, it is the ratio of the strength of its stipe or holdfast (whichever is weaker) to the stress (force/cross-sectional area where force is experienced) from hydrodynamic forces. If the ESF is greater than 1, the alga will remain attached to the substratum. If the ESF is less than 1, then the frond will detach. Through morphological variation (Johnson and Koehl 1994) and changes to tissue strength through ontogeny (Stewart 2006), the likelihood of detachment from the substratum can be similar for very different morphotypes of algae, in very different habitats at different stages of their lifecycles across seasons.
Within species differences in morphology in different flow habitats
Many seaweeds exhibit morphological variation in response to water motion (reviewed in Koehl 1986; Hurd 2000; Stewart and Carpenter 2003). Morphological attributes in calm water include undulations (Gerard and Mann 1979; Koehl and Alberte 1988), high surface area/volume ratio (SA/V) (e.g. Littler and Littler 1980; Stewart and Carpenter 2003), and increased length relative to fronds in wave-exposed habitats (Blanchette 1997). These modifications all potentially result in increased light interception, and mass transfer of nutrients and gases to and from the algal frond (Koehl and Alberte 1988), although this has not been established in all cases (Koehl and Alberte 1988; Hurd et al. 1996; Denny and Roberson 2002). Characteristics of algae in wave-exposed sites include flat strap-like blades (e.g. Gerard and Mann 1979) that streamline easily (Koehl and Alberte 1988), and fronds with low SA/V (Stewart and Carpenter 2003), both of which can decrease the hydrodynamic force experienced by the alga and the chance that it will be dislodged from the substratum.
To gain insight into the advantages conferred by aspects of morphology to the frond in its habitat, it is important to quantify the consequences of morphological variation to performance across sites. The hydrodynamic consequences of many of the traits mentioned above have been well studied. Buoyancy is another common trait among benthic algae. Blades of buoyant algae may be kept up at the surface and spread out increasing light interception and photosynthetic rates (Koehl and Alberte 1988). Buoyancy can also reduce the forces experienced by an alga in waves (Stevens et al. 2001; Stewart 2004). However, the effect of buoyancy on survival of benthic algae is less well known.
Objectives of this study
This study was conducted to investigate the effect of buoyancy, in combination with other morphological traits, on the ESF of a tropical benthic alga, Turbinaria ornata, in different flow habitats. T. ornata is a member of the Division Phaeophyta, in the Order Fucales. The genus Turbinaria is pan-tropical, and species T.ornata is common throughout French Polynesia (Payri and N’Yeurt 1997). It thrives in both calm backreef habitats, where flow is unidirectional and relatively slow, and under waves in forereef habitats, where flow is bi-directional and much faster. Dwarfism of fronds on the reef crest has been reported (Stiger and Payri 1999), and fronds in backreef habitats have gas-filled floats (“pneumatocysts”) and are buoyant, whereas fronds in wave-exposed forereef sites either lack pneumatocysts entirely or have very small, rudimentary pneumatocysts and are not buoyant (Stewart 2004).
Specifically this study addresses the questions: (1) Is buoyancy in T. ornata a plastic trait? (2) How do the morphologies of T. ornata from the backreef and from the forereef (including differences in buoyancy and other morphological traits that differ between habitats) affect performance (as measured by ESF)?
Materials and methods
This research was conducted in forereef and backreef habitats near the Richard B. Gump Research Station, University of California at Berkeley, on the island of Moorea, French Polynesia. Adult fronds (those with reproductive structures, but not yet a high load of encrusting epiphytes, as in Stewart (2006) of T. ornata were collected from points selected using a random number table along transects in the forereef and backreef of the barrier reef between Cook’s Bay and Oponohu Bay on the north shore of Moorea. Length of fronds collected ranged from 17-21 cm for backreef fronds and 11–16 cm for forereef fronds. Fronds were held in running seawater in shaded tanks and used within 2 days of collection.
Flow in forereef and backreef
Estimates of the maximum water velocity under waves were made using wave force meters designed to record maximum velocities as described by (Bell and Denny 1994). Three wave meters were attached to eyebolts that were attached with epoxy onto the forereef and collected after 24 h for each of 3 days and the maximum flow velocity measured by each meter was recorded. At the backreef site, the time required for neutrally buoyant particles to travel 45 cm was measured to the nearest 0.1 s to estimate flow speed. Estimates of flow in the backreef were made at midday when the waves on the forereef appeared to be biggest, so that they would correspond to forereef maximum velocity measurements. Five measurements per day were made for 3 days.
Both the material properties of an organism’s tissues and the organism’s size and shape dictate how it deforms in response to an applied load such as hydrodynamic forces. Elastic modulus, 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. 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 broken along the stipe.
The force with which the stipe resisted the extension was measured to the nearest 0.001 N using a strain gauge made of two 120-Ω resistors (Micro-Measurements Group Inc., type CEA-06-062UW-120, PA, USA) glued flush to either side of the stationary beam to which the stipe was attached. Voltages generated from the deformation of the strain gauges via a Wheatstone bridge were recorded using a bridge amplifier (Gould, model 11-4113-01) and the configuration described above. The force transducers were calibrated by hanging weights from a string attached to the beam at the same point that the stipes were 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. 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 experienced by the strain gauges. A linear regression (r2 = 0.86) was established from the linear relationship between voltage and force, with a precision of 0.001 N.
Algae can be exposed to unidirectional or wave-driven flow that results in bi-directional flow along the substratum. The forces experienced by an alga can include drag, acceleration reaction, and inertial. Peak drag forces occur at maximum velocities. Acceleration reaction is highest during high rates of change of velocity. Inertial forces occur when a flexible organism that is moving in the direction of the flow comes to the end of its tether and its mass is suddenly brought to a halt (Denny 1988). In this study I consider only drag forces because backreef fronds are exposed to unidirectional flow where drag forces dominate, and drag should be the dominant force acting on forereef organisms as waves pass (Denny 1995; Gaylord 2000). In the forereef, the displacement of the water in either direction under waves of 8–10 second period is much larger then the length of the algae and they are pulled in one direction and then the other for long periods of time. Work by Gaylord (2000) suggests that the spatial scale of wave-induced accelerations is too small to encompass any alga large enough to be at risk from accelerational force. Additionally, measurements of horizontal force experienced by fronds of T. ornata from both backreef and forereef locations in waves did not exhibit a substantial force at the time that water velocity approached 0 m/s (Stewart 2004), as would be indicative of inertial force (Denny et al. 1998).
Environmental stress factor
The ESF is the ratio of the breaking stress of the stipe at a particular stage in its ontogeny (calculated above) divided by the stress due to drag experienced by the frond in flow velocities experienced during that season in its habitat. I calculated the ESF for forereef and backreef algae for a range of velocities to explore the consequences of the frond morphology to the likelihood of detachment in different flow habitats. Stress experienced in the stipe of algal fronds due to drag was calculated by dividing the mean drag force experienced by forereef and backreef fronds (calculated above) by the mean cross-sectional area for forereef and backreef stipes for flow speeds of 0–12 m/s. The Cd values obtained at the highest flow speeds in the flume (0.6 for forereef algae and 0.5 for backreef algae) were used to calculate ESF at flow speeds faster than those possible in the flume.
Flow in forereef and backreef
Flow on the forereef was faster than in the backreef over the same time period. Flow velocities in the backreef averaged 0.14±0.06 m/s (mean ± SE), while maximum forereef flow velocities averaged 1.04±0.26 m/s. These estimates were made on relatively calm days in winter (the calm season on the north side of Moorea), and therefore are not indications of the maximum velocities at these sites. These measurements are in no way attempts to characterize the complete flow environment of the two sites, however they do provide an example of the relative differences in flow velocities experienced on the forereef and in the backreef.
Morphometrics of backreef and forereef thalli
Thallus length (cm)
Bladed length (cm)
Unbladed length (cm)
Thickness at holdfast (cm)
Blade length (cm)
Blade diameter at stipe (cm)
Distance between blades (cm)
# Total blades
% Blades with pneumatocysts
Proportion survival of transplanted thalli (n=10 for all treatments)
Environmental stress factor
The ESF was higher for forereef fronds than backreef fronds at all flow speeds from 0 to 6 m/s (Fig. 4b). At flow speeds typical of estimates of flow speeds in the backreef on calm days (<1 m/s) the ESF is high (+2.5) for both backreef and forereef fronds, suggesting that on calm days it is unlikely that fronds of either morphology would be swept away by ambient water motion in the backreef. The ESF drops below one for backreef fronds at 1.7 m/s, and at 4.2 m/s for forereef fronds.
Buoyancy of T. ornata
Data from the transplant experiment suggest that the production of pneumatocysts and corresponding increase in buoyant force is a plastic trait that is influenced by flow environment. Buoyant fronds of T. ornata disperse by drifting, with fertile fronds capable of dispersing 100s of km on ocean currents before releasing germlings (Stiger and Payri 1999b). Plasticity in the ability to produce pneumatocysts ensures that new populations of T. ornata in calm habitats can produce buoyant fronds, which can in turn, disperse by drifting. This has proven to be a successful dispersal strategy for T. ornata in, that has been attributed to its increase in abundance and distribution across islands throughout French Polynesia (Payri and Naim 1982; Stiger and Payri 1999b).
Changes to size and shape of existing pneumatocysts associated with environment have been reported for a number of algae. More streamlined shapes and smaller size of pneumatocysts have been reported to correlate with high flow areas in other algae (Brandt 1923; Druehl 1978; Pace 1972; Dromgoole 1981; Norton et al. 1981) suggestive of a drag-reducing response in high flow. The effects of pneumatocysts in altering drag in this study are confounded by the other morphological differences between forereef and backreef algae. However, Stewart (2004) did find that backreef fronds experimentally manipulated to be non-buoyant (while maintaining all other morphological variables) experienced higher horizontal force in moving water than buoyant backreef fronds. Therefore, the absence of pneumatocysts in forereef frond suggests that this is a drag-reducing mechanism. Production of pneumatocysts in low flow suggests that there are advantages to buoyancy when not overshadowed by disadvantages due to hydrodynamic forces in high flow.
It is not clear how expensive, in terms of resources, buoyancy is to produce and maintain in Turbinaria or algae in general. Production of gas-filled pneumatocysts may be a less energetically expensive mechanism of imparting buoyancy than other mechanisms such as oil bodies and ionic regulation (Walsby 1972), but allocation of resources away from blades to air bladders and fertile tissue may result in decreased photosynthetic performance (Kilar et al. 1989). Buoyancy in T. ornata provides a mechanism to maintain backreef fronds in an upright position, which for forereef fronds is accomplished by thick, short stipes, and high flexural stiffness (Stewart 2004). But, its not clear if and to what extent the combination of low tissue strength and high buoyancy, or low buoyancy and high strength might be the result of resource allocation.
Aspects of the morphology of T. ornata from each habitat may contribute to the differences in drag coefficients for these fronds. Increased length of backreef fronds likely contributed to their higher drag coefficients than shorter forereef fronds at low velocities. However, the low flexural stiffness of the stipes of backreef fronds (Stewart 2004) allowed them to bend over toward the substratum where they experienced reduced velocities and force lower in the benthic boundary layer as flow speed increased. Short forereef fronds may find some refuge from high forces lower in the boundary layer on the forereef, but their high breaking stress allows them to cope in this high flow environment. Forereef fronds were thicker in their stipes and at the attachments of blades to the stipe, making them overall more robust than backreef fronds.
The elastic modulus was not statistically significantly different for backreef and forereef fronds indicating that forereef and backreef fronds are stretchy to the same degree. Forereef fronds had higher breaking extension ratios and higher breaking stress than backreef fronds indicating that forereef fronds must be pulled to longer extensions to cause them to break and that they experience higher stress to pull them to such extensions. Because the stipes of forereef fronds are thicker than backreef fronds at the point at which they break (Table 1), the higher breaking stress of forereef fronds is indicative of stronger fronds, as more force is required to break forereef fronds than backreef fronds.
The morphological variation between forereef and backreef fronds results in higher drag coefficients for forereef fronds than backreef fronds at low flow speeds. However, these differences are reduced as flow speeds increase (Fig. 4a). Due to the non-predictable relationship between drag coefficient (CD) and flow speed (Vogel 1994), the estimates of CD are limited to the maximum velocity of the flow tank (0.75 m/s). Extrapolations to higher flow speeds can be unreliable, as algae with strap-like or pliable blades are moved into increasingly streamlined shapes by increasing water velocities (Sheath and Hambrook 1988; Carrington 1990; Stewart and Carpenter 2003) decreasing the forces they experience (e.g. Carrington 1990). However, the unique pinecone-like shape of T. ornata makes it behavior in moving water unlike that of many other macroalgae. The blades of T. ornata do not reorient relative to the stipe, and the frond does not take on a new overall shape, but retains its pine-cone like shape even at the highest flow velocities. Yet, at high velocities whole fronds of backreef T. ornata were pushed toward the substratum and may experience slower flow lower in the boundary layer at high flow speeds.
Environmental stress factor
The ESF calculated here are based on measurements of drag, and it is possible that the oscillatory nature of the flow on the forereef introduces acceleration reaction forces that may play a role in dislodgement of these fronds. Acceleration reaction was not considered here, in part for the reasons in noted in the Drag coefficient section of the methods. However, it is acknowledged that other forces than drag may be affecting the survival of T. ornata in the forereef, and perhaps in the backreef as well during big storms backreef fronds may be exposed to waves that pass over the crest. Drag is certainly a predominant force in both habitats and for this reason estimates of ESF were calculated using drag. However, estimates of ESF for forereef fronds may overestimate the ability of forereef fronds, and perhaps backreef fronds to persist during big storms. A similar approach was taken by (Pratt and Johnson 2002) to determine the ESF for algae exposed to different intertidal wave exposures.
The ESF described above were based on measurements made on healthy adult fronds. The ESF of fronds of backreef T. ornata decreases with age (Stewart in press), with older fronds facing increased risk of detachment than younger fronds. Rafts of T. ornata found floating after storms are composed mostly of mature, old fronds, which have lower breaking stresses than adult fronds (Stewart 2006). This pattern of lower strength and lower ESF for old fronds than young fronds has also been shown for another buoyant alga, the giant kelp Nereocystis luetkeana (Johnson and Koehl 1994). As noted above, dislodgement of buoyant T. ornata fronds is an important dispersal mechanism, and so cannot always be considered detrimental to the survival of a frond.
Advantages of site-specific morphologies of fronds of T. ornata
Aspects of the morphology of fronds typical of the backreef and the forereef may confer advantages specific to their habitats. Because T. ornata needs hard substrate for attachment, attachment of backreef algae is limited to patches of dead coral on bommies separated by sand. Since settlement space is limited on these small patches, dense aggregations of T. ornata occur on such patches, and competition for light interception may arise between fronds. Long, buoyant fronds that protrude to the tops of aggregations are not shaded as severely as short ones (Stewart unpublished data), and frond length and buoyancy increase light interception within aggregations. As backreef fronds experience relatively low water motion, damage by hydrodynamic forces may be less of a concern for these algae than light interception. In addition, flow velocities may be reduced inside aggregations of T. ornata (Stewart unpublished data), as has been shown in kelp forests (e.g. Eckman 1987, 1989; Jackson 1997) and seagrass (e.g. Fonseca et al. 1983). Reduction of flow in algal assemblages can reduce the force that fronds experience within the assemblage (Johnson 2001), further reducing the chance of breakage of backreef fronds.
Forereef fronds of T. ornata are one of few organisms (in addition to encrusting coralline algae and some corals) that are able to persist under breaking waves on the forereef. The substratum in this region is composed primarily of coral pavement, and T. ornata is a dominant organism in this habitat. This is perhaps one of few places on a coral reef that there is not intense competition for space or light, and fronds of T. ornata do not grow in dense aggregations on the forereef, but spread out over the substratum. Therefore, the morphology of forereef algae may be shaped more by hydrodynamic force than are backreef algae, and the shape and material properties of forereef algae of T. ornata, particularly its strength, has enabled it to persist in this habitat.
This study has shown that aspects of morphology differ between backreef and forereef habitats, and that one aspect of morphology of T. ornata, the production of pneumatocysts and resulting buoyancy is a phenotypically plastic trait in response to water motion. Forereef algae are stiff, negatively buoyant, strong, and experience high drag forces, and backreef algae are buoyant and weak. Yet, the morphology of backreef and forereef fronds confers advantages to survival in their respective habitats, and the chance of detachment may be similar for forereef and backreef fronds.
I thank M. Koehl for advice and guidance, T. Cooper and G. Wang for help with equipment construction, and A. Stewart, J. You-Sing, and T. You-Sing for help in the field. Special thanks to C. Payri for sharing her knowledge of the natural history of T. ornata and Polynesian reef ecology, and to two reviewers for improving the overall quality of this manuscript. Funding was provided a PEARL fellowship from the University of California Richard B. Gump South Pacific Research Station, a post-graduate fellowship from the Natural Science and Engineering Research Council (NSERC) of Canada, and a Ralph I. Smith Fellowship to H. L. Stewart. NSF grant # OCE-9907120 and #OCE-0241447 to M. Koehl provided additional funding for equipment and supplies. Funding was also provided by National Science Foundation Moorea Coral Reef LTER (OCE-0417412) and The Gordon and Betty Moore Foundation. This is contribution #102 of UC Berkeley’s Richard B. Gump South Pacific Research Station, Moorea, French Polynesia. Experiments conducted in this study comply with the laws of French Polynesia and the United States of America.