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Fig. 8. Forces d required to break adult holdfasts and the holdfast break areas n at two sites in pre- and post-storm sampling dates. Sites are labeled as EXP, wave-exposed site; PRO, wave-protected site. Error bars
are standard error. Asterisks above symbols represent the sampling dates and sites for holdfast break area, pre-storm EXP
,post-storm PRO that are significantly different, 0.01,P0.05 one-way ANOVA.
detached, there was preliminary evidence that the remaining holdfast on the rock was attached less firmly. However, sample sizes were too small for statistical analyses;
therefore, it can not be concluded that partial removal affects the integrity of the remaining holdfast.
Even though analysis of attachment properties using one-way ANOVA showed no differences in average attachment forces among sites and seasons Fig. 8, there is a
seasonal effect on the distribution of attachment forces within the sampled populations. Despite no change in holdfast size, within each site, there is a shift to more resistant
holdfasts as a result of increased seasonal wave-exposure Fig. 10. For simplicity, 95 confidence intervals Table 4 are not shown around the estimated distributions in Fig.
10; however, above the normalized force of 1.5, there is a seasonal effect at each site P
,0.05 towards more resistant holdfasts where the post-storm population had a lower probability of removal than the pre-storm population.
4. Discussion
4.1. Juvenile attachment Data presented here are the first to suggest that flow regime and holdfast substratum
K .L.D. Milligan, R.E. DeWreede J. Exp. Mar. Biol. Ecol. 254 2000 189 –209
203
Fig. 9. Relationship between holdfast and wetted blade surface area. Each data point represents an individual thallus sampled for holdfast attachment at exposed dm and protected sn sites in pre-storm ds and
post-storm mn dates. Solid wave-exposed site and dashed wave-protected site lines are the regression lines for the significant, direct relationships between holdfast area and the wetted blade surface area that it
supports refer to Table 3 for the correlation statistics and sample sizes.
interactions are potentially important factors for determining juvenile survivorship and abundance. Hedophyllum sessile juveniles occur more often on articulated coralline
algae AC than on other available substrata and this difference is more distinct in the exposed site, as evidenced by differential recruitment estimates.
An organism’s attachment force to the substratum can be increased by two mechanisms: by an increase in strength and or by an increase in attachment surface area.
Table 3
a
Analysis of wetted blade surface area per holdfast area Sample group
Wetted blade surface area n
R P value
holdfast area ratio 695 CI
Exposed, pre-storm 157.10
666.49 15
0.67 0.007
Protected, pre-storm 167.90
654.41 18
0.84 ,0.001
Exposed, post-storm 62.27
615.19 21
0.65 0.001
Protected, post-storm 76.98
613.21 33
0.75 ,0.001
a 2
2
Normalized blade area was calculated by the ratio between wetted blade area m and holdfast area m . 95 confidence intervals were calculated as in Cochran 1977. Pearson correlation coefficients, R, and
associated probabilities were calculated for the relationship between holdfast area and wetted blade surface area illustrated in Fig. 8. Post-storm samples have significantly p
0.05 less blade biomass per holdfast area than pre-storm samples.
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Fig. 10. Cumulative functions for probability of holdfast dislodgment. Each data point represents the observed normalized attachment forces f at exposed dm and protected sn sites in pre-storm ds and
n
post-storm mn dates. Solid wave-exposed site and dashed wave-protected site lines are the calculated probability distributions from Eq. 3 for each sample date as noted. Equation coefficients
695 CI are given in Table 4.
Hedophyllum sessile juveniles had a significantly greater attachment force on AC algae in the exposed site than in the protected site. On AC, juveniles in the exposed site had
less holdfast area and consequently greater strength than the juveniles in the protected site. Thus, these results demonstrate that H
. sessile juveniles have an increased total
Table 4 Coefficient values
695 CI for the cumulative distributions for the probability of breaking Hedophyllum sessile holdfast attachments in exposed E and protected P sites in pre- and post-storm months see Eq. 3
for description of the coefficients Coefficient
E, pre-storm P, pre-storm
E, post-storm P, post-storm
a 20.38060.268
20.12060.133 20.07060.181
0.300 60.160
b 21.49060.406
20.97460.187 20.82860.295
20.34060.200 c
0.662 60.045
0.663 60.025
0.612 60.039
0.663 60.032
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205
attachment force to the substratum by increased attachment strength rather than by increased holdfast area.
These observed differences in juvenile attachment forces and strengths between sites and substrata types are likely a reflection of physical mechanisms that begin acting at
microscopic stages of development. Rougher surfaces have been shown to provide optimal settlement and growth environments for some species, such as Enteromorpha
sp. Christie and Shaw, 1968 and Sargassum muticum Norton, 1983 by offering refuge from shear forces and more surface rugosity for holdfast development and
attachment. Holdfasts in Laminariales attach by forming microscopic rhizoids from their haptera that fill in crevices on the substratum Tovey and Moss, 1978. Thus, any
greater surface roughness and microsurfaces of AC in comparison to other substrata may provide more interstitial areas into which rhizoids may penetrate and thus provide extra
attachment strength force per unit area and total holdfast force.
Previous studies on Hedophyllum sessile recruitment have focused on effects of grazers, specifically the chiton Katharina tunicata, on juvenile distributions and densities
Duggins and Dethier, 1985; Markel and DeWreede, 1998. Articulated coralline algae have upright thallus parts and they form a low
,10 cm turf. H. sessile holdfasts are attached at the base of the turf. In this study, we can not exclude grazer influence as a
potential mechanism of juvenile H . sessile distributions since AC may provide a refuge
from K . tunicata Markel and DeWreede, 1998.
Results here suggest that another possible driving mechanism for this distribution pattern is hydrodynamic stress, because juveniles increase holdfast strength and thus
total attachment force in AC turfs and in correlation with increased wave exposure. Significantly greater attachment force and greater strength of Hedophyllum sessile
juveniles on AC algae in the exposed site than in the protected site indicate a biomechanical response to wave-exposure, whereby more hydrodynamic stress is
reflected in firmer attachment properties. The lack of juveniles on crustose coralline algae CC in the exposed environment, but their presence in the more protected site,
could be explained by the fact that haptera are not attached firmly on CC, which may result in greater dislodgment risks in the exposed site than in the protected site. Given
these findings, the potential for interactive effects between grazing, substratum type, and juvenile holdfast attachment properties on resultant recruitment warrant further in-
vestigations.
4.2. Adult attachment In comparison to other algal taxa for which field attachment forces have been
measured, Hedophyllum sessile has a weak attachment strength, but extremely high attachment force attained by large surface area. This is in contrast to patterns observed in
juvenile populations, where greater attachment force is achieved by increased strength. More than 85 of the adult H
. sessile holdfasts detached completely. The holdfast
22
attachment strength of H . sessile is 0.07 MN m
whereas, for example, the stipe blade
22
attachment strength for Mazzaella linearis and M . splendens is 8–9 MN m
Shaug-
22
hnessy et al., 1996 and for Mastocarpus papillatus is 7 MN m Carrington, 1990.
Despite H . sessile’s low attachment strength, its overall attachment force for complete
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holdfast dislodgment; 100.68 N is substantially higher than other taxa which have been documented, with the exception of kelp species such as Egregia menziesii stipe
break 589 N; Friedland and Denny, 1995.
Gaylord et al. 1994 predicted that large holdfasts are selected against, most likely because they support more biomass. In this study, selection in Hedophyllum sessile was
against large but loose holdfasts and thallus tattering was a common occurrence. Within each site, there was no difference between sampling dates of average holdfast sizes but
the mean blade surface area was lower in the post-storm sampling, which is likely a result of thallus tattering, not of dislodgment. Initially, it was predicted that holdfast size
would be directly correlated to its removal force. Likewise, Norton et al. 1982 found that, in Macrocystis pyrifera, small holdfasts less than 2 years old were less firmly
attached than those older with larger holdfasts. However, our results illustrate that the relationship between size and attachment force is not always directly correlated, and that
a correlation is seasonally dependent as well as size and age-dependent. Larger holdfast surface area did not correlate to higher attachment force in the pre-storm sampling date,
suggesting that holdfasts loosen as they become larger and that, prior to winter storms, large holdfasts are disproportionally weak. In the post-storm sampling, holdfast areas
were significantly correlated to the force required to dislodge them, suggesting that the large but loose holdfasts were removed from the population. This loss of large but loose
holdfasts resulted in the probability of holdfast dislodgment distributions within the populations shifting towards more resistant holdfasts in the post-storm sampling.
Biomass loss by thallus tattering and resistance to detachment by holdfast attachment force varied as a result of increased storm-swells and hence wave-exposure. Variations in
the biomass relative to holdfast attachment force will place different detachment and mortality risks on adult Hedophyllum sessile during hydrodynamic stress. Our results
indicate that biomechanical parameters such as holdfast attachment force and drag forces based on wetted area measured for populations can not be assumed to be
constant. These biomechanical properties will be exposure-specific e.g. with site or seasonal exposure as demonstrated in this study. Future studies should attempt to
document the seasonal variation of biomechanical attributes in macroalgal field populations, especially when these parameters are used to interpret demographic rates
such as survival across a range of sites.
Extensive field sampling to establish how attachment properties vary within popula- tions is labor intensive and destructive. The ability to predict the extent of holdfast-
loosening events would be an important step towards predicting seasonal dynamics of attachment properties. However, mechanisms creating large, loose holdfasts have not
been well quantified. Loosening agents such invertebrate burrowing activities and substratum failure may be important factors contributing to holdfast failure. Even though
interactions between a kelp holdfast’s invertebrate community and the growth of the holdfast have been reported Ojeda and Santelices, 1984; McLay and Hayward, 1987,
the subsequent effects on attachment forces and survival of the kelp have been rarely documented Tegner et al., 1995.
In this study, substratum degradation under larger holdfasts was one likely cause for loose but large holdfasts. Partial substratum failures were responsible for an average of
24 of the complete holdfast dislodgment occurrences and happened when bleached
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207
coralline algae were removed with the Hedophyllum sessile haptera. Assuming that larger holdfasts are older, coralline algae under larger holdfasts may be degraded
sufficiently to increase the chance of holdfast dislodgment by substratum failure.
4.3. Ecological implications: recovery by juveniles after adult removal Studies on thallus dislodgment have demonstrated that removal occurs when hydro-
dynamically-induced force exceeds attachment forces Gaylord et al., 1994; Friedland and Denny, 1995. Biomass loss in Hedophyllum sessile would ultimately reduce stress
on the holdfasts. If dislodgment occurs, H . sessile holdfasts are the most likely location
for failure and will most frequently be completely removed with no chance of regeneration. When adults are removed, part of the failure is at the crustose substratum,
and consequently a patch of bare rock is opened for colonization. It is rare to find juveniles on bare rock in these moderately to highly wave-exposed sites Milligan,
1998; recolonization by H
. sessile may be most successful once coralline algae have re-established from the surrounding area. If articulated coralline algae colonize the open
area, then this will enhance H . sessile recruitment and offer a more secure attachment
surface than crustose coralline algae.
5. Conclusion
