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Physiology and Biochemistry |
2Plant Biomechanics Group, University of Freiburg, Botanic Garden, Schänzlestrasse 1, 79104 Freiburg i. Br., Germany; 3Botany Department, University of Otago, P.O. Box 56, Dunedin, New Zealand
Received for publication March 17, 2006. Accepted for publication July 21, 2006.
ABSTRACT
Seaweeds have a simple structural design compared to most terrestrial plants. Nonetheless, some species have adapted to the severe mechanical conditions of the surf zone. The material properties of either tissue sections or the whole stipe of four wave-exposed seaweeds, Durvillaea antarctica, D. willana, Laminaria digitata, and L. hyperborea, were tested in tension, bending, and torsion. Durvillaea has a very low modulus of elasticity in tension (Etension = 3–7 MN·m–2) and in bending (Ebending = 9–12 MN · m–2), torsion modulus (G = 0.3 MN · m–2) and strength (
brk = 1–2 MN · m–2), combining a compliable and twistable stipe "material" with a comparatively high breaking strain (
brk = 0.4–0.6). In comparison, the smaller stipes of Laminaria have a higher modulus of elasticity in tension (Etension = 6–28 MN·m–2) and in bending (Ebending = 84–109 MN·m–2), similar strength (brk = 1–3 MN·m–2), and a higher torsion modulus (G = 0.7–10 MN·m–2), combined with a lower breaking strain (brk = 0.2–0.3) than Durvillaea. Time-dependent, viscoelastic reactions were investigated with cycling tests. The tested species dissipated 42–52% of the loading energy in tension through plastic-viscoelastic processes, a finding that bears important ecological implications. Overall, there seems to be no correlation between single material properties and the size or habitat position of the tested seaweed species.
Key Words: biomechanics • Durvillaea • Laminaria • modulus of elasticity • Phaeophyceae • tension tests • wave exposure
Seaweed habitats of rocky wave-swept shores
The rocky intertidal zone of exposed temperate coasts is mechanically a very challenging habitat (Denny, 1988
). In the course of evolution, intertidal seaweeds have adapted their morphology and material properties to withstand hydrodynamic forces typical for their respective habitats. Maximum recorded forces in the intertidal range from >25 N for small species [e.g., Pelvetia <1 m long (Gaylord, 2000
)] up to >300 N for large species [D. antarctica >4 m long (Stevens et al., 2002
; Harder et al., 2006
)]. Many intertidal seaweeds can endure these kind of forces for several years [Durvillaea, >9 yr (Hay, 1979
); L. hyperborea, >10 yr (Kain, 1979
)]. Compared to other biological materials, many seaweeds are very flexible and extensible, but weak (Koehl, 1982
; Speck and Schmitt, 1992
; Koehl, 1996
). The size of exposed seaweeds generally correlates with the site-specific wave regime (Denny, 1999
). Typically, smaller intertidal seaweed species tend to dominate more wave-exposed coasts, and within a species, thallus size decreases with increasing wave exposure (see Hurd, 2000
, and references therein).
Temperate intertidal rocky shores of the NE Atlantic and SE New Zealand are dominated by Phaeophycean seaweeds, which grow at distinct vertical positions above low water. In the temperate waters of southern New Zealand, the zone from the mid intertidal to the upper subtidal is dominated by the genus Durvillaea. Durvillaea antarctica (Chamisso) Hariot is anchored in the mid-intertidal, while D. willana Lindauer often grows in close proximity at mean low water springs and is only emersed on low spring tides (Hay, 1994
). In the NE Atlantic, Laminaria digitata (Hudson) J. V. Lamouroux is often the dominant species of the lower intertidal. Typically just below this zone, L. hyperborea (Gunnerus) Foslie is emersed on only the lowest spring tides but can also grow at greater depths (
32 m; Emschermann, 1992
). Species of these two genera are among the largest seaweeds that thrive in the wave-dominated intertidal.
Seaweeds growing at different zones on the shore will experience different wave action. Under extreme (e.g., stormy) conditions flow rates of up to 25 m · s–1 and accelerations >400 m · s–2 have been recorded in the surf zone of wave-swept rocky shores. The upper subtidal encounters, on average, lower velocities and acceleration magnitudes than the intertidal, and hence less potential for flow-induced damage and mechanical failure (Gaylord, 1999
; Denny and Gaylord, 2002
; Denny et al., 2003
). The Durvillaea and Laminaria species tested in this study grow on rocky shores with moderate to severe wave climates. Comparing their typical habitats, a gradient of exposure is suggested, with L. hyperborea growing under comparatively benign conditions, L. digitata and D. willana occupying an intermediate position, and D. antarctica, thriving under conditions too extreme for the other species.
The overall morphologies of the four tested seaweeds are similar but can vary within species (Fig. 1), and there may be differential adaptations of mechanical properties of individuals to the local wave regime (McEachreon and Thomas, 1987; Harder et al., 2004
, 2006
). Both genera have a holdfast, long stipe, and large blade, but Durvillaea is considerably larger and bulkier than Laminaria (Hay, 1994
). The blade of D. antarctica is typically 4–7 m long and develops a buoyant internal medullary honeycomb structure (Naylor, 1953
). The stipe of D. willana is longer than that of D. antarctica and has lateral blade-bearing branches. The blade of D. willana lacks the honeycomb structure and is subsequently less bulky than D. antarctica (Hay, 1994
) but of similar length. Laminaria hyperborea is up to 4 m long, with a stipe length of often >1 m (Kain, 1979
). Laminaria digitata, the smallest of the tested seaweeds with a typical length of 2–4 m, has a shorter and thinner stipe than L. hyperborea (Kain, 1979
). Overall, there is a great variability in the morphology of seaweeds, although morphological parts like holdfast, stipe, and blade are simple in their structural design compared to terrestrial plants.
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; Naylor, 1953
).
Mechanical testing
Applying standard test methods used by engineers has provided useful insights into the way biological structures are set up in response to specific physical conditions (Niklas, 1992
; Speck et al., 1996
; Herrel et al., 2006
). Wave-imposed loads will act on a stipe in bending as well as in pure tension. Additionally, the lamina is often moved in a circular or elliptical fashion by waves normal to the stipe axis, subjecting the stipe to a torsional load. An analysis of the mechanical properties of stipitate seaweeds should therefore consider both types of mechanical loading.
Aim of the study
There have been numerous studies examining how seaweeds or higher plants are adapted mechanically to their physical environment on different structural levels (e.g., Speck et al., 1990
, 2001
, 2003
; Biehle et al., 1998
; Speck and Spatz, 2001
; Hoffmann et al., 2003; Speck and Rowe, 2003
). In this study, we present information on the mechanical properties of the stipes of Durvillaea and Laminaria as a possible reflection of structural adaptations to different degrees of wave-induced loadings. In particular, three hypotheses were tested: (1) A more severe wave climate will, on average, generate higher forces on the thallus. A stronger wave exposure should therefore coincide with higher breaking stresses of the crucial morphological structure of the thallus, i.e., the stipe. (2) Drag is a major component of the mechanical load. Reconfiguration is an effective way of reducing drag and thus the mechanical load. A low bending stiffness can facilitate an alignment with flow-generated forces acting on the kelp. The more severe the average wave exposure, the lower the bending stiffness is expected to be. (3) The direction of successive wave forces can vary considerably over short periods of time. Therefore, the ability to streamline as quickly as possible is facilitated by a low torsional rigidity and should decrease with more wave action.
MATERIALS AND METHODS
Seaweed collection
Stipes of Laminaria digitata (N = 10) and L. hyperborea (N= 13) were harvested by SCUBA divers in Helgoland, Germany, near the harbor wall, between May and August 1998. They were transported to the laboratory at Freiburg, Germany, in an ice box within 2 days. Stipes of D. antarctica (N = 40) and D. willana (N = 26) were harvested from Brighton Beach, Otago, New Zealand, during low tide between April 1998 and January 2000. They were transported to the laboratory at the University of Freiburg in an ice box within 3 days. All stipes were stored in the laboratory in seawater-soaked newspaper for up to 3 weeks at 4°C without obvious signs of deterioration. Control tests conducted in Helgoland, Germany, and Dunedin, Otago, New Zealand, with freshly harvested material indicated no effect due to transport and storage.
Mechanical analysis of excised tissue strips
Tension tests
To determine the main load-bearing structure of Laminaria and Durvillaea stipes, the mechanical properties of the medulla and cortex were compared. Tension tests (Koehl and Wainwright, 1985
; Biehle et al., 1998
) were conducted with an Instron universal testing machine (Instron Wolpert GmbH, Ludwigshafen, Germany) and a custom-built portable tension machine with a 50 N force transducer (Plant Biomechanics Group, Freiburg, Germany). The initial distance between the grips was always 20 mm, and strain rates were between 0.1 and 0.4 min–1. Test samples that were 1–2 mm thick were excised with a vegetable peeler and trimmed to a testing length of 20 mm and a width of 1–2 mm (aspect ratio 
10; cf. Fig. 2). The dimensions of the section between the grips of the tension machine were measured with calipers to the closest 0.1 mm. Three readings of the thickness and the width of the test sample were averaged to calculate the rectangular cross-sectional area. The cut ends of the sample within the grips were wider to ensure firm gripping during testing and were wrapped with paper towel to prevent slipping (Vincent, 1992
). This method was checked by tracking specimens with a dissecting microscope to see if slipping occurred. Specimens that broke near the grips (<1 mm) were discarded from the analysis of fracture mechanics because tissue damage due to clamping could not be ruled out.
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brk [MN·m–2], and breaking strain brk [m/m] could be determined. Typically, there was a linear part at low strains, which was recorded as initial E1 and a second linear part of the stress-strain curve at high strains, which was recorded as a second modulus of elasticity E2 for comparison (Fig. 3). As an additional comparison, whole stipes were also tested.
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There are gradients in cell size and tissue mechanical properties across the stipes of Laminaria and Durvillaea (see Harder et al., 2000
). Therefore, to represent equal proportions of the cross-sectional tissue distribution, the diameter of each stipe was measured, and up to eight approximately equidistant sections from the periphery to the central part of the respective tissue were tested. The results were then pooled as either cortex or medulla. Based on these initial tests, the cortex tissue was considered the main load-bearing structure; subsequently, cortex samples were used for interspecific comparisons (see Results; Niklas, 1994
).
Viscoelastic processes
An analysis of the time-dependent behavior was conducted with cycling experiments. The start of a new loading cycle yielded another linear part of the stress–strain curve recorded as cyclic modulus of elasticity, Ecycl, which was then analyzed semi-quantitatively by calculating the ratio of E1/Ecycl. To examine plastic and viscoelastic processes, specimens were loaded to a pre-defined stress of approximately = 1.2 MN·m–2, representing a lower estimate of the breaking stress of the four tested seaweed species. The moving direction of the cross-beam of the tension testing machine was then reversed and the specimens were unloaded to zero stress, and the cyclic loading was repeated. The under-curve areas, representing the different types of work, were analyzed with Optimas, using the same method as for the work per volume.
Mechanical analysis of whole stipes
Bending and torsion experiments
The stipes of the two Laminaria species and the two Durvillaea species were subjected to four-point-bending in a custom-built bending apparatus (Rowe and Speck, 1996
; Ennos et al., 2000
; Rowe et al., 2006
). Straight stipes (overall length > 20 cm), with little taper, and an aspect ratio (L/d) > 15 were selected and tested in bending. Subsequently, the stipes were placed in seawater-soaked newsprint in a cool box and stored for subsequent testing in torsion. The weight–deflection relation was used to determine the flexural rigidity in four-point-bending (Roark and Young, 1975
).
The stipes used in the bending experiments were also tested in torsion with a custom-made torsion balance (Ennos et al., 2000
; Gallenmüller et al., 2001
). The stipes were clamped at both ends with the mountings approximately 20 cm apart, with the exact distance measured to the closest 1 mm. The lower mounting was made of an outer grip connected to an inner mounting via an exchangeable spring, which had in our experiments a stiffness of 0.00241 Nm·rad–1. The stipes were subjected to a torsional load by twisting the lower grip in 10° increments until reaching a maximum torsional deflection of 120°. The spring in the lower mounting allowed measurement of the resistance of the stipe to twisting, and the deflection was recorded after a settling time of 30 s. The long and short cross sectional diameter at the base, the mid section, and the apex were measured with calipers to the closest 0.1 mm. The cross-sectional shape was assumed to be elliptical, and the polar second moment of area was calculated with the mean of the three respective diameters. The torsional rigidity, GJ, of the stipes was calculated (in N · m · rad–1) as:
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| (1) |
o is the displacement of the outer mounting and i is the displacement of the inner mounting in radians.
Statistical analysis
All statistical analyses were performed with SPSS (version 11.0, SPSS Inc., Chicago, Illinois, USA) and R (version 1.6.1, http://www.r-project.org). Intraspecific differences of the mechanical properties of the cortex and medulla tissues of Laminaria and Durvillaea were examined by Welch's two sample t-tests, assuming unequal variances between samples. Interspecific differences in mechanical properties of all tested species were determined by Welch's ANOVA, assuming unequal variance between samples, and were always confirmed by nonparametric Kruskal–Wallis tests. If a significant difference between groups was detected, post hoc Tamhane's t tests (P < 0.05), assuming a non-normal distribution and unequal variances, were performed.
RESULTS
Mechanical analysis of excised tissue strips
Intraspecific comparison: tension tests of the cortex and medulla
Neglecting the lag phase, the initial modulus of elasticity was obtained by a linear regression (r2 > 0.98) of the first linear part of each stress–strain curve. The intersection of the regression line with the x-axis was taken as the corrected point of zero elongation.
The initial moduli of elasticity were low and ranged on average from E1 = 3–7 MN·m–2 for all tested species (Table 1). The medulla of L. digitata, L. hyperborea, and D. antarctica had a significantly lower E1 than the cortex (Welch's t test, P < 0.05; Table 1) and was therefore more compliant, whereas for D. willana, the moduli of elasticity of the cortex and the medulla were very similar. On average, the medulla of all four tested species also had a lower modulus at high strains, E2, than the cortex, but was significantly different only for D. antarctica (Welch's t test, P < 0.05; Table 2). For all species tested, the means of the strength of the cortex were higher than for the medulla, but the two tissues could be separated at a significant level only for D. antarctica (Welch's t test, P < 0.05; Table 1) and L. hyperborea (Welch's t test, P < 0.05; Table 1). The breaking strain was similar in both tissues for all tested species and no significant difference could be detected (Welch's t test, P > 0.05; Table 1). The work of fracture per volume was significantly higher in the cortex than the medulla only for D. antarctica (Welch's t test, P < 0.05; Table 1). Overall, the cortex was stiffer and stronger. Subsequent comparisons therefore focused on the cortical tissue as the mechanically most important structural element within the stipe. Although variations in the mechanical properties might vary with seasons, at least for Durvillaea, no significant differences in stiffness, breaking strain, or breaking strength were found (D. Harder, unpublished data).
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The analysis of the fracture mechanics yielded an average breaking stress ranging from brk = 1.5–3.2 MN·m–2, and no significant difference between species could be detected (Welch's ANOVA, P > 0.05; Table 1). Comparing the breaking strain, both Durvillaea species (brk = 0.5–0.6 m/m) were about three times and significantly more extensible than the Laminaria species (brk = 0.20 m/m; Welch's ANOVA, Tamhane's t test, P < 0.05; Table 1). The general pattern observed for the work of fracture per volume mirrored those of the breaking strain (Table 1). Laminaria hyperborea required the lowest amount of energy before failure and significantly less than D. antarctica or D. willana. Also, L. digitata had a significantly lower work of fracture than D. antarctica (Welch's ANOVA and Tamhane's t test, P < 0.05). Although the mean (W/V]brk was higher for D. antarctica than for D. willana and also higher for L. digitata than for L. hyperborea, no significant difference could be detected between the two congeneric species.
Mechanical properties of whole stipes in tension
Comparing the stiffness at two levels of analysis, the tension tests of small whole stipes (integral level) yielded values for the modulus of elasticity comparable to the tension tests with cut-out cortex tissue strips (Table 1). Durvillaea was on average more compliant than Laminaria. While the tissue strips yielded very similar moduli of elasticity for the Laminaria species, the whole stipes of L. digitata were on average more compliant than the whole stipes of L. hyperborea, although the two species could not be statistically separated at a significant level. Laminaria hyperborea was significantly stiffer than the two Durvillaea species (Welch's ANOVA, Tamhane's t test, P < 0.05). Comparing the tests of tissue strips and entire stipes, the mean stiffness of the stipes of L. hyperborea was higher than for the cortex tissue strips, and lower for L. digitata, D. willana, and D. antarctica, although a significant difference could only be detected for the last species (Welch's t test, P < 0.05; Table 1).
Viscoelastic processes
The time-dependent mechanical behavior was analyzed in detail with cycling experiments. With the four tested seaweeds, the size of the hysteresis loop did not change significantly after the first loading cycle so that the amount of plastic deformation energy for the second cycle was considered negligible. All samples were stiffer in the second loading. Most remarkably, the ratio of E1/Ecycl (0.6–0.7) was very similar for all tested species. The cycling experiments allowed the quantification of the plastic and viscoelastic proportions of the energy dissipation. With all four tested seaweeds species, the amount of dissipated energy for the first cycle (viscoelastic-plastic) was between 40–50% (Fig. 4). The amount of dissipation was on average highest for D. antarctica and significantly lower for L. digitata (Welch's ANOVA, Tamhane's t test: P < 0.05), with D. willana and L. hyperborea being intermediate. For the second (mainly viscoelastic) cycle, the amount of dissipated energy was very similar for the four tested species with about 14–17% of the total deformation work (Fig. 4).
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The torsion experiments yielded similar low torsion moduli for D. antarctica, D. willana, and L. digitata (Table 2). The highest G was recorded for L. hyperborea (G = 10 ± 5 MN·m–2), which was significantly higher than for Durvillaea (Welch's ANOVA, Tamhane's t test: P < 0.01; Table 2).
DISCUSSION
Mechanical analysis on the tissue level
Regarding the elastic properties on the tissue level, the elastic moduli for the cortex are well within the range of values reported in other studies on a broad scope of seaweed species (e.g., the red algae Chondrus crispus [E = 18 MN·m–2] or Mastocarpus stellatus [E = 26 MN·m–2]; Dudgeon and Johnson, 1992
), or the brown algae Hedophyllum sessile (E = 4.0–9.7 MN·m–2), and Postelsia palmaeformis (E = 6.4–0.5 MN·m–2; Holbrook et al., 1991
; Gaylord et al., 1994
). Comparable moduli of elasticity in terrestrial plants have been found in nonlignified parenchyma of Cyclamen sp. (E = 20 MN·m–2), Solanum tuberosum (E = 5–20 MN·m–2), or Zea mays (E = 20 MN·m–2). The absence of stiff structural components like lignin makes algal tissue compliant compared to many other biological materials, and although interspecific differences are present, they are small regarding the whole spectrum of stiffness of plant materials (Speck and Schmitt, 1992
).
The modulus of elasticity is defined as the slope of the first linear part of a stress–strain curve (Vincent, 1992
) and is usually used as a means of comparison of elasticity between different seaweed species (Koehl, 1986
; Dudgeon and Johnson, 1992
), but from an ecological perspective, it may be well justified to focus on the second, high-strain modulus E2. This second modulus can be observed in many marine and terrestrial plants species (Koehl and Wainwright, 1985
; Holbrook et al., 1991
; Johnson and Koehl, 1994
; Speck et al., 1998
; Koehl, 2000
; Köhler et al., 2000
; Keckes et al., 2003
) and may be characteristic for biological composite materials (Spatz et al., 1999
). It can be expected that algal stipes experience high strains in situ fairly frequently and subsequently react to forces in the mode of the high-strain modulus, E2.
Many brown seaweed species typically have low breaking stresses, compared to terrestrial plants, in spite of their wide spectrum of morphologies and habitats. Values of brk = 1–5 MN·m–2 have been reported for a range of macroalgae. These low values may therefore represent a developmental constraint in Phaeophyta and seaweeds in general, indicating that the strengths of seaweeds cannot be modified on a large scale by a wide range of ambient physical conditions, although plastic responses and subsequent changes of mechanical properties on a small scale, triggered by applied forces, are possible (Kraemer and Chapman, 1991
). This is in contrast to terrestrial plants in which factors like light or physical contact can trigger a change of an order of magnitude in the mechanical properties (e.g., in lianas; Gallenmüller et al., 2001
; Speck et al., 2003).
Compared to terrestrial plants, seaweeds are extremely extensible. Wood can be typically stretched to a strain of about brk = 0.01 (Niklas, 1992
; Speck and Schmitt, 1992
), whereas seaweeds can be further extended by one to two orders of magnitude (e.g. the brown algae Ascophyllum nodosum [brk = 0.5; Lowell et al., 1991
], Hedophyllum sessile [brk = 0.5; Armstrong, 1987
], or Pterygophora californica [up to brk = 0.75; Biedka et al., 1987
]). These high breaking strains, however, are often only found for tissue strips. Whole stipes will commonly fail at lower strains, as surface nicks and scars in combination with the brittle nature of algal material makes them prone to crack propagation, causing them to snap (Santelices et al., 1980
; Holbrook et al., 1991
). Notably for D. antarctica, a breaking strain of whole stipes of brk = 0.17 was found by Koehl (1986)
and by Smith and Bayliss-Smith (1998)
. Therefore, although the stipe as a whole is still far more extensible than equivalent structures of terrestrial plants, the excision of tissue strips can lead to an overestimate of the breaking strain.
During the second loading, all tested seaweeds typically reacted more stiffly than during the first loading. Because of the oscillatory nature of wave-induced loads, this kind of induced structural stiffening may be an ecologically very important factor. Seaweeds probably react to hydrodynamic forces with pre-loaded stiffness, Ecycle, and not with the modulus of elasticity usually taken from the first, previously unloaded phase of tension experiments, E1.
Mechanical analysis of whole stipes
The values for the bending modulus of elasticity are notably larger than the tensional modulus of elasticity. This somewhat surprising result has also been found in studies on Postelsia palmaeformis (Holbrook et al., 1991
; Gaylord and Denny, 1997
) and was attributed to either the differences in preparation technique and/or population characteristics.
A major difference in the mechanical properties of the tested species is the way their stipes react to twisting. The cross-sectional shape of the stipes of the tested seaweeds is often elliptical, in particular with D. antarctica and L. digitata (Oltmann, 1922
; Hay, 1979
). Although the stipes of adult Durvillaea are considerably more voluminous than the stipes of Laminaria (Harder et al., 2004
), their torsional rigidity is notably low. Due to the low torsional rigidity, excessive bending stresses can partly be avoided by rapidly twisting the stipe so that the shorter diameter of the stipe is normal to the main force. The stipe can subsequently be bent quickly and align with the force, bearing partially the load in tension and thus reducing maximum stresses and strains associated with bending.
The torsion tests provide a very useful base for the comparison of the type of behavior of seaweeds to terrestrial plants subjected to dynamic lateral loads. On an absolute scale, the values of G are very low compared to most terrestrial plants. They are comparable to some vines, plants that are optimized to twist easily (Gallenmüller et al., 2001
), as for Wisteria sinensis, which has a torsion modulus of 105 MN·m–2 (Vogel, 1995
). Compared to the corresponding specific bending moduli of elasticity, the torsion moduli are also very low and are similar to findings for petioles of the banana Musa textilis (Ennos et al., 2000
) or the sedge Carex acutiformis (Ennos, 1993
) with EI/GJ ratios between 40 and 100. It seems therefore justified to assume that for intertidal seaweeds, twisting is a particularly important way of reacting to wave action since the typical findings for the seaweed species in this study are among the extremes for terrestrial plants. This result therefore supports hypothesis 3, that a low torsional rigidity facilitates rapid streamlining in heavily exposed seaweeds.
Conclusion
Compared to other intertidal organisms, the tested stipitate seaweeds are exceptionally large (Denny et al., 1985
). Wave-induced loads will often result in a combination of torsion, bending, and pure axial tension of the stipe. Regarding the uniformly low breaking strengths of the tested species, hypothesis 1 can be discarded because no differences in breaking strengths could be detected between samples.
Kelp with higher wave exposure can align more rapidly with major flow forces by being compliant in bending and/or torsion. Moreover, time-delayed mechanical reactions of seaweeds may be an important factor for the survival of high dynamic loads that are typical for the intertidal (Gaylord et al., 2001
). The results of this study support hypotheses 2 and 3, because the most wave-exposed species, D. antarctica, has the lowest E and G as well as the highest amount of energy dissipation, whereas the least wave-exposed species L. hyperborea has the highest E and G. For more detailed analyses, new and additional protocols need to be developed as well as the means to record the actual forces in the field, the ones acting on the seaweeds and those that are actually experienced by the kelp (Harder et al., 2000
; Stevens et al., 2002
). In conclusion, no single mechanical property is obviously correlated with the size or habitat position of the tested seaweed species.
FOOTNOTES
1 The work was funded by the Royal Society of New Zealand Marsden Fund to C.L.H., an Otago Research Grant (MFC B11) to C.L.H., and by the DAAD and a traveling grant to D.L.H. in the course of a Procope project grant to T.S. and N.P. Rowe (Montpellier). The authors are grateful for technical support from the Technical Workshop, University of Freiburg and field assistance from the Alfred Wegener Institute, Helgoland. 
4 Author for correspondence (deane.harder{at}biologie.uni-freiburg.de
), phone: ++49-761-2302877; fax: ++49-761-2302880
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