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Variation in Anatomical and Material Properties Explains Differences in Hydrodynamic Performances of Foliose Red Macroalgae (Rhodophyta)1

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Variation in Anatomical and Material Properties Explains Differences in Hydrodynamic Performances of Foliose Red Macroalgae (Rhodophyta)1 J. Phycol. 47, 1360–1367 (2011) Ó 2011 Phycological Society of America DOI: 10.1111/j.1529-8817.2011.01066.x VARIATION IN ANATOMICAL AND MATERIAL PROPERTIES EXPLAINS DIFFERENCES IN HYDRODYNAMIC PERFORMANCES OF FOLIOSE RED MACROALGAE (RHODOPHYTA)1 Kyle W. Demes2 Department of Zoology, University of British Columbia, 6270 University Blvd. Vancouver, B.C., Canada V6T 1Z4 Emily Carrington Friday Harbor Laboratories, Department of Biology, University of Washington, Friday Harbor, Washington 98250, USA John Gosline Department of Zoology, University of British Columbia, 6270 University Blvd. Vancouver, B.C., Canada V6T 1Z4 and Patrick T. Martone Department of Botany, University of British Columbia, 6270 University Blvd. Vancouver, B.C., Canada V6T 1Z4 Over the last two decades, many studies on Key index words: biomechanics; blade; cortex; functional morphology have suggested that material flexural stiffness; medulla; Rhodophyta properties of seaweed tissues may influence their Abbreviation: EI, flexural stiffness fitness. Because hydrodynamic forces are likely the largest source of mortality for seaweeds in high wave energy environments, tissues with material properties that behave favorably in these environ- ments are likely to be selected for. However, it is Seaweeds have an intricate relationship with water very difficult to disentangle the effects of materials velocity. While submerged, increased flow facilitates properties on seaweed performance because size, acquisition of CO2 and nutrients for growth and shape, and habitat also influence mechanical and productivity (Hurd et al. 1996, Cornelisen and Tho- hydrodynamic performance. In this study, anatomi- mas 2006). However, moving water also imposes cal and material properties of 16 species of foliose drag forces on seaweeds, calculated as follows: red macroalgae were determined, and their effects 2 on hydrodynamic performance were measured in F ¼ 1=2qv ACd ð1Þ laboratory experiments holding size and shape con- stant. We determined that increased blade thickness where F = drag, q = density, v = velocity, A = pro- (primarily caused by the addition of medullary jected area, and Cd = drag coefficient. Seaweed tis- tissue) results in higher flexural stiffness (EI), which sues must be stronger than the hydrodynamic forces inhibits the seaweed’s ability to reconfigure in flow- they experience to avoid dislodgement and ing water and thereby increases drag. However, this subsequent mortality. Seaweeds are able to resist increase is concurrent with an increase in the force hydrodynamic forces by strengthening their tissues required to break tissue, possibly offsetting any risk (Lowell et al. 1991, Martone 2007) or by reducing of failure. Additionally, while increased nonpig- the area exposed to flowing water by remaining mented medullary cells may pose a higher metabolic small or by reconfiguring (Vogel 1984, Koehl and cost to the seaweed, decreased reconfiguration Alberte 1988, Armstrong 1989, Carrington 1990, causes thicker tissues to expose more photosynthetic Boller and Carrington 2006) to become more surface area incident to ambient light in flowing hydrodynamically streamlined. While seaweed water, potentially ameliorating the metabolic cost of strength and reconfiguration potential (indexed by producing these cells. Material properties can result flexibility) are both dependent on tissue material in differential performance of morphologically simi- properties, little is known about how seaweeds pro- lar species. Future studies on ecomechanics of sea- duce materials of varying properties. weeds in wave-swept coastal habitats should consider Unlike terrestrial plants, which produce multiple the interaction of multiple trade-offs. tissue types for different structural roles (Kokubo et al. 1989, Vincent 1991), macroalgae are usually limited to pigmented cortical cells at the tissue sur- 1Received 27 September 2010. Accepted 6 May 2011. face and nonpigmented medullary cells in the tissue 2Author for correspondence: e-mail [email protected]. center. The cortical cell layer is comparable among 1360 FUNCTIONAL MORPHOLOGY OF RED BLADES 1361 most species, comprising one to several layers of other seaweed biomechanical studies have high- tightly packed photosynthetic cells. Medullary tissue, lighted the importance of tissue material properties on the other hand, varies greatly among taxa in (i.e., strength, extensibility, bendiness, etc.) on terms of thickness, degree of compaction, and cell hydrodynamic performance (Lowell et al. 1991, shape (Fritsch 1959). Although medullary cells are Johnson and Koehl 1994, Gaylord and Denny 1997, responsible for the translocation of photosynthate Harder et al. 2006, Boller and Carrington 2007). in kelps (Schmitz and Lobban 1976), in red macro- Despite recent advances in this field, a paucity of algae (Rhodophyta), connections between medul- data exists describing (i) variation in material lary cells are blocked by proteinaceous pit plugs properties among species (although see Koehl (Pueschel 1989), leaving their function unclear. 2000), (ii) how variation in material properties is Despite the wide-spread prevalence of nonpig- produced by the individual (however, see Martone mented medullary tissue among red macroalgae, 2007), and (iii) how differences in material proper- little is known about its function. However, the ties affects seaweed fitness. addition of medullary cells may have significant While previous comparative studies have provided biomechanical consequences for seaweeds. Most important insight into how differences in biome- importantly, increasing tissue thickness should chanical properties (strength, flexibility, and EI or increase breaking force and EI (Vogel 2003), both bendiness) may affect the fitness of marine organ- of which likely affect seaweed fitness. EI is the resis- isms, it is very difficult to disentangle the relative tance of an object to bending and is defined as the effects of species identity, size, shape, and environ- product of a material’s modulus of elasticity (E) and ment. Furthermore, how internal growth form and its second moment of area (I). Increasing tissue thallus construction affect tissue material properties thickness should not affect E but will greatly affect I, is almost entirely unexplored in these studies (how- which increases with thickness cubed (Vogel 2003). ever, see Koehl 1999, Martone 2007). All else being equal, thicker blades will be stiffer Foliose red macroalgae (Rhodophyta) provide and therefore less easily reconfigured. Likewise, the an excellent way to tease apart the aforementioned addition of medullary cells may decrease the ability confounding factors and explore effects of tissue of seaweeds to reconfigure, thereby exposing them construction on material properties because of the to higher hydrodynamic drag forces, which may in abundance of taxonomically distinct blades, which turn have negative effects on fitness. can be distributed growing next to one another. The ability of macroalgae to reconfigure in flow- While all red blades are often lumped into the ing water and thereby reduce drag is known to be functional group ‘‘foliose macroalgae’’ (Steneck ecologically important (Koehl 1984, Carrington and Dethier 1994), it is possible that many differ- 1990). However, only recently have researchers ent thallus constructions and tissue types could attempted to quantify differences in reconfiguration produce a bladed morphology. In this study, we potential among species and found that stipe bendi- quantify material properties of 16 species of foliose ) ness, (EI) 1, is largely responsible for this process red macroalgae. We controlled size and shape in turf-forming seaweeds (Boller and Carrington in the laboratory to test the effects of material 2006). Most species converge on similar maximally properties on hydrodynamic performance. Specifi- reconfigured shapes at high velocities that are rep- cally, we ask: (i) Do differences in material proper- resentative of exposed intertidal sites (M. L. Boller ties exist among foliose red macroalgae? (ii) If and P. T. Martone, unpublished data); however, variation in material properties exists among spe- large differences in reconfiguration potential occur cies, are anatomical differences responsible for ) among species at lower velocities (<2 m Æ s 1) that such variation? (iii) Does variation in material are representative of protected, high-current- properties explain differences in hydrodynamic exposed, or subtidal sites. Reconfiguration may performance? come at the metabolic cost of self-shading, present- ing an interesting trade-off between maximizing MATERIALS AND METHODS photosynthetic surface area incident to light (pro- ductivity) and minimizing hydrodynamic drag forces Specimen collection and processing. Table 1 lists the taxonomic placement and collection locality of species used in this study through reconfiguration (hydrodynamic forces) (identifications by and authorities available through Gabriel- (Koehl and Alberte 1988, Koehl et al. 2008). son et al. 2006). Because variation in material properties within Hydrodynamic forces imposed by strong currents a species has been shown to result from environmental factors and breaking waves have been proposed to be a (Armstrong 1987, Kraemer and Chapman 1991, Kitzes and strong selective pressure in shaping the evolution of Denny 2005), care was taken to collect specimens from intertidal organisms (Denny 1988). Likewise, a locations of similar exposure. All collections were made within the San Juan Islands (Washington,
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