|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online February 15, 2006
Journal of Experimental Biology 209, 881-890 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02050
Seasonal influence of wave action on thread production in Mytilus edulis
Department of Biological Sciences, University of Rhode Island, Kingston, RI 02881, USA
* Author for correspondence at present address: Friday Harbor Laboratories, University of Washington, Friday Harbor, WA 98250, USA (e-mail: gmmoeser{at}u.washington.edu)
Accepted 20 December 2005
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: mussel, Mytilus edulis, byssal thread, flow, temperature
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Carrington and Gosline, 2004).
Mussels form dense assemblages that not only help secure their own survival,
but also buffer other organisms from the physical stresses of the intertidal
zone (Bertness and Leonard,
1997). As dominant competitors and important bioengineers, mussels
exhibit a strong influence on the diversity and structure of the intertidal
community (Paine, 1974;
Suchanek, 1978).
Mytilus edulis Linnaeus, the blue mussel, tethers itself to the
substrate by producing a byssal complex composed of multiple extracellular
collagenous byssal threads. Each thread is secreted by a gland in the foot in
a manner similar to polymer injection molding, and terminates at an adhesive
plaque which attaches the thread to the substrate
(Waite, 1992). By varying the
number of threads produced, M. edulis may be able to influence the
strength of its attachment (Bell and
Gosline, 1997; Carrington,
2002a). Along with thread number, variations in the mechanical
quality and the rate at which threads decay may also influence mussel
attachment to the substrate (Bell and
Gosline, 1996; Moeser,
2004).
Flows produced by large breaking waves generate hydrodynamic forces (drag
and lift) on organisms in the intertidal zone
(Bell and Gosline, 1997;
Denny, 1987;
Denny, 1988;
Witman and Suchanek, 1984). A
mussel will be dislodged from the substrate when these forces exceed its
attachment strength (Carrington,
2002a; Carrington,
2002b; Denny et al.,
1985). Storms represent one of the largest survival risks for
intertidal mussels because these events increase wave action over a period of
1–2 days and can quickly dislodge individuals with weak attachment. In
the North Atlantic, extreme storms such as hurricanes have increased in
frequency and severity since 1995
(Goldenberg et al., 2001).
Mean wave height has also increased by 2% per year over the latter half of the
20th century (Bacon and Carter,
1991; Hoozemans and Wiersma,
1992). If these trends continue, hydrodynamic forces within the
intertidal zone are predicted to increase concomitantly, thereby increasing
dislodgement rates, unless mussels can increase their attachment strength
(Carrington, 2002a;
Helmuth et al., 2005).
A twofold annual variation in attachment strength, or tenacity, has been
observed for M. edulis on both Rhode Island, USA and British rocky
shores (Carrington, 2002a;
Price, 1980;
Price, 1982). Price
(Price, 1982) found that peak
mussel attachment preceded storm seasons, suggesting that mussels anticipated
increases in wave action by increasing attachment strength. However,
Carrington (Carrington, 2002a)
observed a different pattern on Rhode Island shores, with attachment strength
peaking during late winter and early spring. In this case, increased
attachment strength followed a period of increased wave action caused by
hurricanes and winter storms and coincided with reduced reproductive effort
and water temperature (Carrington,
2002a). This most probably reflects a strengthening of the entire
population of mussels rather than a distributional shift due to fall-off of
weak mussels (Carrington,
2002a). Since this increase in attachment strength occurs at a
different time in the East Atlantic compared to the West Atlantic, it is
difficult to determine which, if any, environmental or physiological factors
influence this variation.
`Wave action' is a qualitative term that refers to small-scale turbulence
superimposed on a directional current that is created by waves breaking on the
shore (Bell and Denny, 1994;
Denny, 1988). Intense wave
action creates extreme hydrodynamic forces which, in turn, increase the risk
of mussel dislodgment (Bell and Gosline,
1997; Carrington,
2002a; Denny,
1987; Hunt and Scheibling,
2001). Wave action exposes mussels to three potential stimuli for
increased thread production: (1) mean flow, (2) acceleration (vertical
displacement of the mussel body) and (3) hydrodynamic loading of the byssal
retractor muscle by transferring tension from the byssal complex. Of these
potential stimuli, flow is presently thought to be the primary cue for
increased thread production in M. edulis
(Dolmer and Svane, 1994;
Lee et al., 1990;
Van Winkle, 1970;
Witman and Suchanek, 1984;
Young, 1985). Previous
research has suggested a positive linear relationship between water flow and
mussel attachment (Dolmer and Svane,
1994). However, mussels held firmly against the substrate exhibit
poor thread production, even under high water velocities
(Seed and Suchanek, 1992);
suggesting that flow is not the only factor influencing thread production. The
response of mussels to agitation, the combination of both acceleration and
byssal loading, has been examined to a lesser extent, with conflicting
results. Van Winkle (Van Winkle,
1970) determined that increased agitation of Geukensia
demissa led to a 33% decrease in thread production when compared with
stationary mussels, whereas Young (Young
1985) suggested that thread production increases notably with
increased rate of agitation in M. edulis. Thus it is unclear how
agitation, and more specifically acceleration and byssal loading, affect
thread production and attachment strength in M. edulis.
The purpose of this study is to identify whether wave action influences thread production thereby driving the temporal variation in the attachment strength of M. edulis on Rhode Island shores. Three aspects of wave action (flow, acceleration and byssal loading) were simulated in the laboratory to determine which stimulus, or combination thereof, was most important in cueing thread production. Flume experiments were also performed to detail the relationship between thread production and flow, and thread production was monitored in the field, seasonally. Together, these experiments indicate that mussels do not respond to wave action with increased thread production and that other explanations for seasonally variable attachment strength warrant further investigation.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
) or Black
Point (1 km south of Bass Rock) in Rhode Island Sound, USA. For the simulated
wave action experiment, mussels were collected from the locations listed
above, however, length varied from 30–50 cm in the two factor
experiments; length was used as a covariate in applicable statistical
analyses. Mussels were held in laboratory aquaria at ambient temperature for
1–4 days prior to experimentation; only mussels that produced greater
than three threads during this acclimation period were chosen as subjects.
Because mussel attachment strength may depend on mussel condition
(Carrington, 2002a), gonad
index (GI) and condition index (CI) were measured for each subject as follows.
Shell length was measured with vernier calipers to the nearest mm, and then
the mantle, including the gonads, was separated from the remaining body tissue
for each mussel. The mantle and the remaining body tissue were then dried to a
constant weight at 60°C (1–2 days). GI was calculated as the dry
mantle mass divided by the total dry tissue mass
(Carrington, 2002a). CI was
calculated as the total dry tissue mass divided by the shell length cubed
(Baird, 1958), where shell
length cubed was used as a proxy for volume
(Bell and Gosline, 1997).
Wave and water temperature conditions were monitored at Bass Rock throughout the study. A SBE26 Seaguage (Seabird Electronics, Bellevue, WA, USA) was mounted at a depth of 7 m approximately 200 m offshore. The sensor recorded temperature every 15 min and burst measurements of pressure (1024 points at 2 Hz) every 4 h. The pressure data were processed with Seasoft software (Seabird Electronics, Bellevue, WA, USA) to obtain significant wave height (Hs) of each burst. Daily averages of water temperature and Hs were calculated for comparison with experimental data.
Statistical analyses for the simulated wave action experiments were performed using SAS 9.0 statistical software (Cary, NC, USA); all other data were analyzed using SigmaStat 3.1 (Systat; Richmond, CA, USA).
|
). Mussels were
fed Post-Set 1800 Shellfish Diet (Reed Mariculture, Campbell, CA, USA) 5 days
per week. An algal biomass equivalent to approximately two percent of the
average dry mussel body mass per mussel per day was distributed to the mussels
using a slow release drip feeder. The experimental water velocities were below
the level where the filtering ability of mussels is severely impeded
(Newell et al., 2001). Each pneumatic pump was equipped with six racks, each containing four mussels and every combination of two components of wave action: acceleration and byssal loading (Fig. 1C). The right valve of each mussel was fixed to a vertical nylon rod using cyanoacrylate glue, which was then suspended 6.5 mm above an acrylic plate (Fig. 2). Preliminary experiments indicated that the suspension of mussels above the substrate did not significantly hinder thread production (G.M.M., unpublished data; H.L., unpublished data). Mussels were aligned with anterior ends downstream to remove any effects of orientation and each was randomly assigned to a three-factor treatment.
|
(1) Flow
Unidirectional flow was established at approximately 8 cm
s–1 (low flow) and 20 cm s–1 (high flow) in
two tanks by circulating water with a transom-mount motor (Minn Kota Endura
40, Sidney, NE, USA; Fig. 1A).
Water velocity was measured at mussel height between each rack using a Marsh
McBirney 511 flowmeter (Frederick, MD, USA). Although the high flow treatment
is well below velocities reported in the field
(Hunt and Scheibling, 2001),
preliminary studies indicated that velocities greater than 20 cm
s–1 reduced thread production to impractical levels (G.M.M.,
unpublished data).
(2) Acceleration
The vertical rod attached to the mussel was connected to an inner support
attached to the aluminum rack support which was oscillated ±2.5 mm at a
frequency of 1.25 Hz by the pneumatic pump system
(Fig. 1B,C), generating a
maximum acceleration of approximately 0.10 m s–2. Although
the magnitude and frequency of this acceleration is lower than field
measurements (Gaylord, 1999),
preliminary trails determined this displacement and frequency maximized the
response without hindering the mussels' ability to contact the substrate
(G.M.M., unpublished). For those mussels experiencing no acceleration, the
vertical rod was attached to a fixed support
(Fig. 1C).
(3) Byssal loading
The distance between the mussel and the acrylic plate was oscillated
±2.5 mm by displacing either the plate or the mussel. This placed a
fluctuating, tensile load of approximately 0.15 N on the mussel byssus, a load
well within the range expected in the field
(Bell and Gosline, 1996). The
control treatment for this experiment consisted of low flow and the absence of
both acceleration and byssal loading. A second set of control mussels
confirmed that mussels attached to the racks were not affected by the motion
of neighboring treatments (Moeser,
2004). For each treatment, mussels were stimulated continuously
for 48 h to maximize mussel response
(Moeser, 2004). The number of
byssal plaques attached to each acrylic plate was then counted, byssal threads
were cut and removed, and mussels were rotated to another treatment. A total
of 48 mussels were rotated through each of the eight treatments over the
16-day experiment. Each mussel was considered a replicate for each treatment
and independent from other mussels. This experiment was performed in two tanks
and relied on pseudoreplication to create two flow regimes; separate controls
failed to identify any tank effects on the ability of mussels to produce
threads (Moeser, 2004).
Mussel GI and CI were estimated, as described above, at the close of each
experiment. Neither of these indices significantly decreased during the
experiments compared to controls; in preliminary analyses of the effect of GI,
CI and mussel length on thread production, only the latter was found to be
significant (Moeser,
2004).
The three factor, full factorial experiment was performed in August, February and October. Data were analyzed separately for each month as a univariate (number of threads produced), fixed factor (flow, acceleration and byssal loading), repeated measures three-way ANOVA with a full factorial design (P=0.05). Data were also analyzed as a univariate (number of threads), mixed factor (month, flow, acceleration and byssal loading) four-way ANOVA with a full factorial design (P=0.05). Owing to the difficulty of maintaining multiple replicate treatments, six additional experiments examined byssal loading and acceleration only. These two-factor experiments were performed at low flow (approximately 8 cm s–1) and mussels were handled as described above (N=24). Data were analyzed as a univariate (number of threads produced), fixed factor (acceleration and byssal loading), repeated measures two-way ANOVA with a factorial design using mussel length as a covariate.
Seasonal thread production data were compared to field measurements of
tenacity at Bass Rock. The latter were obtained from monthly measurements of
intertidal mussels, averaged over a 6-year period, 1998–2003 (data from
Carrington, 2002a; E.C.,
unpublished data). Regression analysis was used to evaluate the influence of
seasonal thread production on tenacity.
Flume experiment
A flume study was conducted to evaluate the thread production response of
mussels to a range of unidirectional water velocities, 5–20 cm
s–1. In July 2004, a circulating flow tank
(Grace, 2004) was used to
expose solitary mussels to a constant water velocity while byssal thread
production was monitored over a 24-hour period. Each of ten mussels was
mounted on nylon rods as described above. Each rod was attached to a rack that
was placed flush with the floor of the working section of the flow tank (120
cmx17 cmx17 cm; LxWxH). Mussels were suspended 6.5 mm
above the substrate, anterior facing downstream and separated by at least one
shell length. Threads produced by each mussel were cut and counted every 24 h
and the mussels were returned to the flume for another velocity trial. A total
of ten trials were run at seven velocities; the velocity order was randomized
among trials and mussels were replaced after 5 days. Seawater in the flume was
aerated at 19°C and changed daily. A time-lapse video camera was used to
observe mussel gaping and foot extension behavior. Nonlinear regression
analysis was used to evaluate the effects of water velocity on mean byssal
thread production.
Field experiment
Byssal thread production by mussels exposed to field conditions was
quantified with a short term (4–5 day) assay repeated during nine spring
low tides from October 2003 to July 2004. The byssus was gently cut from each
of twenty mussels and shells were cleaned of byssal attachments. Each mussel
was loosely tethered to an acrylic plate (5.3 mm thick; approximately 25 cm
square) using a short length of braided nylon line (20 kg test). The line was
affixed to each valve of the mussel using cyanoacrylate glue and further
secured with marine epoxy (Devcon, Riviera Beach, FL, USA). The braided line
was then threaded through pre-drilled holes 
2 cm apart and tied off on
the underside of the acrylic plate. A temporary 5.3 mm spacer was used to
ensure uniform slack in each tether. Four mussels were mounted on a total of
five replicate plates; mussels were spaced a minimum of 4 cm apart with their
anterior-posterior axis parallel to the plate.
Screws and plastic wall anchors were used to secure the plates with the attached mussels to a 1 m2 horizontal area in the middle intertidal mussel zone at Bass Rock. Thread production was quantified daily by counting the adhesive plaques on the transparent plate and on the mussels themselves. Thread production rate (per day) was calculated as total threads divided by the assay duration. After 4–5 days, each mussel was dissected and weighed to determine the GI and CI as described above.
Differences in thread production rate among assay dates were evaluated using an ANOVA on square-root transformed data. A forward stepwise regression was used to predict mean thread production from the following mussel condition and environmental parameters: GI, CI, water temperature and Hs. Mussel condition indices were average values for each assay; environmental parameters were average daily mean values recorded during the assay. The criterion for parameter entry was P<0.05 for an F-test of the hypothesis that the parameter coefficient was zero.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
|
|
In the remaining experiments, conducted under low flow conditions, acceleration and byssal loading had only a minor influence on thread production (Table 2). Specifically, the effects of these two factors were significant only in early June (P<0.01, byssal loading) and late June (P<0.01, accelerationx load interaction; Fig. 5). In contrast, all other experiments failed to demonstrate a significant effect of either acceleration or byssal loading on thread production. When the data are pooled by month, a clear seasonal pattern is observed with elevated thread production in summer. This pattern roughly corresponds to annual cycles in water temperature, GI and CI (Fig. 6). However, none of these potential factors were significantly correlated with thread production in the laboratory (P= 0.06–0.58).
|
|
|
Flume experiment
Byssal thread production by mussels exposed to constant flow varied
nonlinearly as a function of water velocity
(Fig. 7). A second order
polynomial regression fit the data well (r2=0.96), peaking
at 10.6 cm s–1. The first and second order coefficients were
both significant (P<0.05), indicating a curvilinear relationship.
Foot extension, which is necessary for thread formation, was visibly hindered
at velocities >18 cm s–1; high flow dragged the foot
downstream and caused premature foot retraction.
|
Field experiment
Mussels produced threads steadily during each 4–5 day deployment, but
this rate of production (total threads per day) varied significantly among
assay dates (Table 3;
P<0.001). Specifically, thread production was significantly lower
in February and March, with the rate three to four times higher in all other
months. Three independent variables were entered into the stepwise multiple
regression analysis of thread production
(Table 4); CI was not entered
because of colinearity with GI. Water temperature explained the greatest
proportion of the variation in the dependant variable (59%), with increased
temperature correlated with increased thread production. Wave height
(Hs) and GI accounted for substantially lower proportions
of the variation in thread production (<20%). Thread production was
positively correlated with GI, but negatively correlated with wave height.
Together, the three variables combine to explain over 90% of the variation in
thread production, with maximal values predicted for conditions with elevated
temperature, reduced wave action, and high mussel reproductive condition.
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The strong response to increased flow contradicts the results of previous
studies on M. edulis, most probably because the latter have focused
on the differences in thread production at only two velocities
(Dolmer and Svane, 1994;
Maheo, 1970;
Van Winkle, 1970). The flume
experiment illustrated that thread production increased concurrently with
flow, up to 10 cm s–1, then decreased as flows continued
towards 20 cm s–1 thus demonstrating that the relationship
between flow and thread production is not linear. Video footage indicates that
mussels had difficulty maintaining the proper foot extension to produce
threads at higher velocities (>18 cm s–1) due to premature
retraction. This inability to maintain contact with the substrate is most
probably driving the curvilinear trend. A similar pattern was observed for the
zebra mussel, Dreissena polymorpha, where thread production peaked at
velocities of 20 cm s–1
(Clarke and McMahon,
1996a).
The bell curve pattern probably explains discrepancies between this study and other `positive' flow effects. Depending on which two flow levels are chosen, a positive, neutral, or negative correlation will be observed. This underscores the need to measure at more than two levels to detect relationships described by second order polynomials; more than two points are required to define a peak.
In addition to flow, byssal loading generally decreased thread production
while the effect of acceleration was inconsistent and sporadic across months.
These results are not surprising, as previous studies have also found that
agitation, the combination of byssal loading and acceleration, produces
conflicting responses in mussels. Young
(1985) observed a marked
increase in thread production following the agitation of M. edulis,
whereas, in D. polymorpha, byssal thread production was found to be
both reduced and enhanced in response to agitation
(Clarke and McMahon, 1996b;
Rajagopal et al., 1996). The
inconsistent response to byssal loading across months observed in this study
is most probably due to the variable amount of load that was experienced by
each individual mussel, which was directly proportional to the number of
threads produced by the mussel and placed in tension. Therefore, mussels that
produced more threads experienced a higher level of byssal loading than those
that produced fewer threads.
While thread production was not enhanced by wave action, it did vary
seasonally, corresponding to changes in environmental and physiological
conditions. Field experiments indicate that 90% of the variation in thread
production can be predicted from changes in temperature, wave height and
reproductive condition; temperature explains the largest amount of the
variation. Similar observations have been made previously
(Allen et al., 1976;
Clarke and McMahon, 1996c;
Young, 1985) suggesting that
temperature may be a better predictor of thread production in mussels than
wave action. However, it is unknown whether temperature is the underlying
mechanism driving this change or another factor that varies concomitantly with
temperature. For example, both nutrient abundance and salinity vary seasonally
with sea surface temperature, therefore, either of these factors could be
driving the variation in thread production
(Carrington, 2002a).
Carrington found that increased tenacity was significantly correlated with
increased thread number and proposed that elevated thread production following
hurricane season leads to stronger attachment in the winter
(Carrington, 2002a). However,
this model was based on a regression analysis largely driven by three points;
high tenacity was frequently associated with lower thread numbers. Both the
laboratory and field data from this study indicate that more threads are being
produced when mussels are most weakly attached to the substrate
(Fig. 8); these periods
coincide with elevated temperature and reproductive effort, and reduced wave
height. Therefore, increased tenacity in winter is not the result of increased
production as suggested (Carrington,
2002a), but instead may be the product of stronger individual
threads that are more decay resistant. Thus, a reduced `shelf life' in summer
could reconcile the patterns observed by this study and Carrington
(2002a). This suggests that
indeed, seasonal variation in byssal thread quality and rates of decay warrant
further investigation (Moeser,
2004).
|
;
Hoozemans and Wiersma, 1992)
and, more specifically, the incidence and strength of hurricanes has increased
significantly within the past 10 years in the North Atlantic Basin
(Goldenberg et al., 2001;
Webster et al., 2005). Since
hurricane season coincides with the period of weakest attachment, the
inability of mussels to respond positively to wave action could severely
increase dislodgement. This increase in hurricane activity also occurs
concomitantly with an increase in sea surface temperature
(Webster et al., 2005), which
is represented not only by a change in local temperature, but has also
manifested itself as changes in wave height, precipitation and other
atmospheric conditions, seasonal patterns, and even nutrient abundance
(Helmuth et al., 2005).
Because these factors are interconnected, it is difficult to predict how
mussels will respond to changes in any single environmental variable
(Helmuth et al., 2005). While our results indicate that thread production is hindered at higher velocities, mussels are still able to securely attach to wave-exposed surfaces during periods of higher flows. When do mussels produce threads? Perhaps, high intertidal flows are significantly dampened within dense mussel beds, or mussels produce threads only when flows are low, such as during slack tides. A more detailed measure of water flow within mussel beds along with observations of thread production in the field would provide insight into this issue.
Although the literature has focused on the integration of wave action and thread production as the primary process affecting mussel attachment strength, this study shows that even modest wave action decreases thread production. More specifically, we have shown that the relationship between flow and thread production is not linear, and that water temperature is the environmental variable that best explains seasonal changes in thread production. Future studies should examine how byssal thread material properties, and their dependence on environmental and physiological conditions, influence mussel attachment strength.
|
Acknowledgments |
|---|
|
Footnotes |
|---|
Present address: Department of Zoology, University of Hawaii, Manoa,
Honolulu, HI 96822, USA 
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Allen, J. A., Cook, M., Jackson, D. J., Preston, S. and Worth,
E. M. (1976). Observations on the rate of production and
mechanical properties of the byssus threads of Mytilus edulis L.
J. Molluscan Stud. 42,279
-289.
Bacon, S. and Carter, D. J. T. (1991). Wave climate changes in the North Atlantic and North Sea. Int. J. Climatol. 11,545 -558.
Baird, R. H. (1958). Measurement of condition in mussels and oysters. J. Cons. Perm. Int. Explor. Mer 23,249 -257.
Bell, E. C. and Denny, M. W. (1994). Quantifying wave exposure: a simple device for recording maximum velocity and results of its use at several field sites. J. Exp. Mar. Biol. Ecol. 181,9 -29.[CrossRef]
Bell, E. C. and Gosline, J. M. (1996). Mechanical design of mussel byssus: material yield enhances attachment strength. J. Exp. Biol. 199,1005 -1017.[Abstract]
Bell, E. C. and Gosline, J. M. (1997). Strategies for life in flow: tenacity, morphometry, and probability of dislodgment of two Mytilus species. Mar. Ecol. Prog. Ser. 159,197 -208.
Bertness, M. D. and Leonard, G. H. (1997). The role of positive interactions in communities: Lessons from intertidal habitats. Ecology 78,1976 -1989.[CrossRef]
Carrington, E. (2002a). Seasonal variation in the attachment strength of blue mussels: Causes and consequences. Limnol. Oceanogr. 47,1723 -1733.
Carrington, E. (2002b). The ecomechanics of
mussel attachment: From molecules to ecosystems. Integr. Comp.
Biol. 42,846
-852.
Carrington, E. and Gosline, J. M. (2004). Mechanical design of mussel byssus: Load cycle and strain rate dependence. Am. Malacol. Bull. 18,135 -142.
Clarke, M. and McMahon, R. F. (1996a). Effects of current velocity on byssal-thread production in the zebra mussel (Dreissena polymorpha). Can. J. Zool. 74, 63-69.
Clarke, M. and McMahon, R. F. (1996b). Effects of hypoxia and low-frequency agitation on byssogenesis in the freshwater mussel Dreissena polymorpha (Pallas). Biol. Bull. 191,413 -420.[Abstract]
Clarke, M. and McMahon, R. F. (1996c). Effects of temperature on byssal thread production by the freshwater mussel, Dreissena polymorpha (Pallas). Am. Malacol. Bull. 13,105 -110.
Denny, M. W. (1987). Lift as a mechanism of patch initiation in mussel beds. J. Exp. Mar. Biol. Ecol. 113,231 -245.[CrossRef]
Denny, M. W. (1988). Biology and the Mechanics of the Wave-Swept Environment. Princeton, NJ, USA: Princeton University Press.
Denny, M. W., Daniel, T. L. and Koehl, M. A. R. (1985). Mechanical limits to size in wave-swept organisms. Ecol. Monogr. 55,69 -102.[CrossRef]
Dolmer, P. and Svane, I. (1994). Attachment and orientation of Mytilus edulis L. in flowing water. Ophelia 40,63 -74.[Medline]
Gaylord, B. (1999). Detailing agents of physical disturbance: wave-induced velocities and accelerations on a rocky shore. J. Exp. Mar. Biol. Ecol. 239,85 -124.[CrossRef]
Goldenberg, S. B., Landses, C. W., Mestas-Nunez, A. M. and Gray,
W. M. (2001). The recent increase in Atlantic
hurricane activity: Causes and implications. Science
293,474
-479.
Grace, S. P. (2004). Coral-macroalgalInteractions in Narragansett Bay. Kingston: University of Rhode Island.
Helmuth, B., Kingsolver, J. G. and Carrington, E. (2005). Biophysics, physiological ecology, and climate change: Does mechanism matter? Annu. Rev. Physiol. 67,177 -201.[CrossRef][Medline]
Hoozemans, F. M. J. and Wiersma, J. (1992). Is mean wave height in the North Sea increasing? Hydrogr. J. 63,13 -15.
Hunt, H. L. and Scheibling, R. E. (2001). Predicting wave dislodgment of mussels: Variation in attachment strength with body size, habitat, and season. Mar. Ecol. Prog. Ser. 213,157 -164.
Lee, C. Y., Lim, S. S. L. and Owen, M. D. (1990). The rate and strength of byssal reattachment by blue mussels (Mytilus edulis L.). Can. J. Zool. 68,2005 -2009.
Maheo, R. (1970). Etude de la pose de l'activite de secretion du byssus de Mytilus edulis L. Cah. Biol. Mar. 11,475 -483.
Moeser, G. M. (2004). Environmental Factors Influencing Thread Production and Mechanics in Mytilus edulis. Kingston: University of Rhode Island.
Newell, C. R., Wildish, D. J. and MacDonald, B. A. (2001). The effects of velocity and seston concentration on the exhalant siphon area, valve gape and filtration rate of the mussel Mytilus edulis. J. Exp. Mar. Biol. Ecol. 262,91 -111.[CrossRef]
Paine, R. T. (1974). Intertidal community structure: Experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15, 93-120.[CrossRef]
Price, H. A. (1980). Seasonal variation in the strength of byssal attachment of the common mussel Mytilus edulis L. J. Mar. Biol. Assn. UK 60,1035 -1037.
Price, H. A. (1982). An analysis of factors determining seasonal variation in the byssal attachment strength of Mytilus edulis. J. Mar. Biol. Assn. UK 62,147 -155.
Rajagopal, S., Van der Velde, G., Jenner, H. A., Van der Gaag, M. and Kempers, A. J. (1996). Effects of temperature, salinity and agitation on byssus thread formation of zebra mussel Dreissena polymorpha. Netherlands J. Aquat. Ecol. 30,187 -195.[CrossRef]
Seed, R. and Suchanek, T. H. (1992). Population and community ecology of Mytilus. In The Mussel Mytilus: Ecology, Physiology, Genetics, and Culture (ed. E. G. Gosling), pp.87 -169. New York: Elsevier.
Suchanek, T. H. (1978). The ecology of Mytilus edulis L. in exposed rocky intertidal communities. J. Exp. Mar. Biol. Ecol. 31,105 -120.[CrossRef]
Van Winkle, W. (1970). Effect of environmental factors on byssal thread formation. Mar. Biol. 7, 143-148.[CrossRef]
Waite, J. H. (1992). The formation of mussel byssus: anatomy of a natural manufacturing process. In Results and Problems in Cell Differentiation, vol. 19. Biopolymers (ed. S. T. Case), pp. 27-54. Berlin: Springer-Verlag.[Medline]
Webster, P. J., Holland, G. J., Curry, J. A. and Chang, H.
R. (2005). Changes in tropical cyclone number, duration, and
intensity in a warming environment. Science
309,1844
-1846.
Witman, J. D. and Suchanek, T. H. (1984). Mussels in flow: Drag and dislodgement by epizoans. Mar. Ecol. Prog. Ser. 16,259 -268.
Young, G. A. (1985). Byssus-thread formation by the mussel Mytilus edulis: Effects of environmental factors. Mar. Ecol. Prog. Ser. 24,261 -271.
This article has been cited by other articles:
|
|
 |
|
  S. L. Brazee and E. Carrington Interspecific Comparison of the Mechanical Properties of Mussel Byssus Biol. Bull., December 1, 2006; 211(3): 263 - 274. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. M. Moeser and E. Carrington Seasonal variation in mussel byssal thread mechanics J. Exp. Biol., May 15, 2006; 209(10): 1996 - 2003. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
