title for learn-about section of A SNAIL'S ODYSSEY
  black dot

Mytilus californianus & other mytilids

  This section deals with anchoring by byssus threads in west-coast Mytilus californianus & other mytilids. An introductory section on anchoring in the Atlantic coast species MYTILUS EDULIS, about which more is known, is presented in another section.
Research study 1

graph comparing forces to detach mussels of different species from rocks: Mytilus californianus and M. trossulusphotograph of mussels Mytilus californianus & M. trossulusComparisons of sea mussels Mytilus californianus and bay mussels M. trossulus in California and British Columbia show that attachment strength in the former is greater than in the latter, whether mussels are solitary or aggregated into beds.  In the Santa Barbara area of California, for example, sea mussels of 25cm2 shell area require about 3 times more force to remove than equivalent-sized bay mussels.  Harger 1970 The Veliger 12: 401. Photo of Mytilus trossulus courtesy Dave Cowles and Walla Walla University, Washington rosario.wallawalla.edu.

Research study 2

photograph of byssus thread attachments to aquarium glass by mussels Mytilus sp.photographs of different types of cilia in the pedal groove of a mussel as compared with the epithilium of the footResearchers at the University of Washington describe 4 major steps in attachment of byssus threads by a mussel Mytilus californianus to the glass side of an aquarium: 1) the tip of the foot extends and gropes about, 2) the depression at the end of the pedal groove is applied firmly to the glass, 3) after a few moments a semi-transparent turbid material appears between the depression and the glass, and 4) the foot retracts to leave an adhesive plaque behind with a single thread attached.  The plaque is in the shape of a flattened oval disc and consists of at least 3 secretions: collagen protein, mucoid material, and polyphenol.  The last two are mixed as a colloidal suspension, with the polyphenol forming the definitive binding material.

Interestingly, the cilia within the the pedal groove of M. californianus are shaped quite differently than other cilia on the foot epithelium.  Whereas the latter have the more familiar rod-shaped appearance, the pedal-groove cilia have biconcave ends and are flattened into “paddles” (see photographs on Right).  The authors think that these cilia may function as microscopic spatulas for application of the viscid adhesive plaque material to the substratum surface.  Tamarin et al. 1974 J Morph 142: 321; Tamarin et al. 1976 J Morph 149: 199.

Research study 3

graphs showing forces required to dislodge mussels at the edge of a bed versus in the centreStudies on wave-exposed shores of Tatoosh Island, Washington show that Mytilus californianus attach much more firmly at the edge of a mussel bed than at the centre (see upper graph on Left).  In wave-protected areas of San Juan Islands, Washington, M. trossulus also exhibits a slight tendency for this (see lower graph on Left). While  both numbers and thickness of threads may be involved, it is known that as a mussel bed grows there tends to be more mussel-mussel attachment instead of mussel-substrate attachment, and this affects mussels in the centre of the bed more than ones at the edges.  A comparison of both species in a wave-exposed location shows, as expected, significantly greater attachment strength representing more than an order of magnitude difference for M. californianus than for M. trossulus (260N vs. 10N, respectively, for individuals with equivalent 8cm2 shell area). Witman & Suchanek 1984 Mar Ecol Progr Ser 16: 259.

NOTE too few data points are available for the authors to calculate a regression line for the centre-of-bed data. However, it is apparent that dislodgement forces are significantly less at the centre than at the edges of the bed

Research study 4

fine-scale comparison of byssus-plaque composition in mussels Mytilus calirornianus and M. edulisAttachment of byssus threads by mussels is, of course, achieved in the presence of moisture, a feat that eludes most synthetic polymers and one that has generated considerable research interest. Analyses of the composition of byssus glue in sea mussels Mytilus californianus collected from Goleta Pier in Santa Barbara, California reveals a primary composition of polyphenolic protein of molecular mass 85,000.  The protein glue is dispersed as a foam from the phenol gland into the distal depression of the foot where it hardens.  A comparison of the porosity of adhesive foam in 2 species, the sea mussel Mytilus californianus from the west coast and the bay mussel M. edulis from Europe shows significantly greater porosity in the latter, suggesting a potential weaker attachment.  This agrees with what is known of actual attachment strengths in the 2 general types of mussels.  Waite 1986 J Comp Physiol B 156: 491.

NOTE  the author provides more detailed description of the protein composition and chemical linking of proteins in the attachment plaques of sea mussels M. californianus in a later publication: Zhao & Waite 2006 J Biol Chem 281 (36): 26150

NOTE see Research Study 5 below

Research study 4.1

photograph of wave-exposed coastline at Botanical Beach, British ColumbiaResearchers at the University of British Columbia compare byssus-thread mechanics of west-coast Mytilus californianus with several other mytilid species. The threads in all species have similar form, each with a proximal corrugated region, a distal smooth region, and an adhesive plaque that attaches the thread to the substratum. The first and last regions are closely matched in strength and are commonly the parts that fail, while the middle, distal region is strongest. It is also the most extensible, which allows it to yield before structural failure occurs. The molecular structure that explains this is, at the time of publication, not known. The distal part of the thread is typically longer in M. californianus than in other mytilid species (80% of total thread length vs. a mean of about 65% for 3 other species: trossulus, galloprovincialis, and edulis). Other features noted by the researchers that increase overall attachment strength of an individual mussel are: 1) orientation of threads is in the direction of applied load (not so evident in M. californianus as in other species because of the turbulent nature of wave stresses in its natural habitat; see photo); and 2) number of threads increases in response to greater load. The second feature distributes the applied load over a larger overall cross-sectional area, thus reducing stress on each individual thread. Comparison of distal-thread morphology and biomechanics with those of mytilid species more constrained to quiet-water habitats suggests that the superior design of threads of M. californianus may be key to explaining its success in wave-swept habitats. Bell & Gosline 1996 J Exp Biol 199: 1005.

NOTE west-coast M. trossulus and M. galloprovincialis, and east-coast/European M. edulis

NOTE the authors’ data show that the distal region is typically twice as strong as the proximal region

Research study 5

histogram showing numbers of byssus threads produced by mussels Mytilus californianus and M. trossulushistogram of attachment tenacities in mussels Mytilus californianus and M. trossulusField studies in Barkley Sound, British Columbia by the same researchers from the University of British Columbia show that although bay mussels produce more threads than California mussels under the same conditions (upper histogram on Right), their threads are 30% thinner (lower graph on Right) and, hence, have lower tenacity (upper graph on Left).graph showing differences in byssus-thread thicknesses in mussel species

In both species, failure of the thread attachment occurs at 3 locations in the following approximate frequencies: root 15%, thread 25%, substratum 60%. Not surprisingly, individuals of both species attach more threads when solitary than when aggregated in beds. Attachment strength, then, at least partly explains why bay mussels are not common in wave-exposed habitats.  In quiet-water areas Mytilus trossulus forms loosely packed clusters that are sometimes easily torn apart.  In contrast, Mytilus californianus in wave-exposed areas form tightly bound, flatter aggregations that maximally resist disruptive wave forces.  This type of close packing actually reduces hydrodynamic loading on individuals, and leads to less stringent requirements for attachment strength.  Production of fewer threads frees up more energy for growth and reproduction. Bell & Gosline 1997 photograph of mussel Mytilus trossulus attaching a byssus threadMar Ecol Progr Ser 159: 197. Photograph courtesy Dave Cowles, Walla Walla University, Washington rosario.wallawalla.edu.

NOTE  production of byssus threads is costly, and accounts for 7-8% of a mussel’s total energy expenditureHawkins & Bayne 1985 Mar Ecol Progr Ser 25: 181.

Bay mussel Mytilus trossulus in the process of attaching a thread to the glass of an aquarium tank. Note that several other smaller threads
are attached to the mussel's own shell 1.4X

Research study 6

photograph of mussels Mytilus trossulus with byssus threads attachedUnder usual circumstances, mussels move very little, if at all.  Studies on tagged Mytilus trossulus in Halifax, Nova Scotia show that in a 4-wk period only 9% of the population moves more than 9cm distance, and most other movements are only about 1-2cm.  Hunt & Scheibling 2002 Veliger 45: 273.

NOTE this species has colonised the north-east Atlantic region, apparently from the Pacific Ocean. In the Atlantic region it hybridises with Mytilus edulis








Bay mussels Mytilus trossulus
with byssus threads 1.4X

Research study 6.1

To what extent does continual stretching of mussel threads through wave action and other forces affect their mechanical properties? Do they ever wear out? These questions and others are addressed for Mytilus californianus and other species by researchers at the universities of photograph of sea mussel Mytilus californianus with byssus threadsRhode Island and British Columbia who cyclically load threads using a tensometer device and measure resiliance (elastic efficiency) and failure levels. Results show that subcritical loading will alter the mechanical properties of byssus threads to an extent dependent on the degree of deformation applied. More interesting are results from dynamic rapid extensions that more closely approximate conditions of wave stress in the field. As expected, the more elastic proximal part of each thread is more stretchable than the stiffer distal part, by a factor of 2 orders of magnitude. Threads will increase in stiffness when cycled repeatedly. Age of thread in this regard does not seem to be involved, as young, freshly produced threads seem to stiffen at about the same rate as older, tanned threads from field animals. Over time, a stiffened thread may cure itself in a kind of “self-healing”, the rate being dependent upon the extent of the original deformation. In practical terms, a hypothetical single-threaded mussel exposed to cyclical wave buffeting on the shore would eventually see its attachment strength compromised to the point of breakage. That this rarely occurs owes to the sharing of loading forces of waves among several to many threads (see photograph). Carrington & Gosline 2004 Am Malacol Bull 18 (1/2): 135.

NOTE other species include M. edulis, M. trossulus, and M. galloprovincialis

Single mussel Mytilus californianus with multiple
byssus threads. Mussels in a bed share wave-
stress loading by attaching threads not just to
the substratum, but also to one another 2X

Research study 7

photograph of byssus plaque of mussel Mytilus californianusAn investigation by researchers at the Marine Science Institute, University California Santa Barbara provides detailed information on the chemical composition of the flattened adhesive plaques of attached byssus threads of mussels Mytilus californianus.  Major components resolve1 into 12 variants of proteins ranging in mass from 5200-6700Da2.  All are highly polar, contain up to 28mol% Dopa3, and are thought by the authors to be the crucial adhesives for wet bonding to metal and mineral surfaces.  The researchers have determined cDNA nucleotide sequences for all 12 variants.   Zhao et al. 2006 The J Biol Chem 281 (16): 11090.

NOTE1  the method used is succinctly described by the authors as matrix-assisted laser-desorption ionization-time of flight-mass spectrometry

NOTE2   a measure of atomic mass, equivalent to 1/12th the mass of the nuclide of Carbon-12

NOTE3   amino acid L-DOPA is formed from L-tyrosine and is a precursor to, among other things, the neurotransmitter dopamine

Research study 8

graphs comparing byssus-thread production in 3 species of west-coast mussels over a range of current speedsgraph comparing water velocities within and without a mussel bedMagnitude of current flow clearly affects the rate of byssus-thread production in mussels.  A study at Friday Harbor Laboratories and at sites around San Juan Island, Washington on 3 mytilid species Mytilus trossulus, M. galloprovincialis, and M. californianus, shows that thread production decreases in flow rates above 25cm . sec-1, with critical flow thresholds being about 50cm . sec-1 (see graphs on Left).  A 4th species included in the study, Modiolus modiolus, usually inhabits subtidal areas, and its production of threads cuts off at much slower flow rates (data not shown here). With this in mind, the authors question how mussels survive on shores with flow rates an order of magnitude higher than 50cm . sec-1.  The answer seems to be in the propensity of mussels to form aggregations.  Measurements of current flows within and above mussel aggregations in the laboratory and in the  field show that flow is greatly reduced within photograph showing how plaster rods dissolve in current flows at different rates depending on the velocity of the currentaggregations, to <1cm . sec-1, or 0.2-0.5% of open-stream velocity (see graph above Right showing flow velocities for mussels of 25mm shell length). The more tightly packed the aggregation, the greater the magnitude of reduction in current speed.  Carrington et al. 2008 Integr Comp Biol 48: 801.

NOTE  individuals of this species are obtained from mussel aquaculturists in Puget Sound, Washington.  The mussels are mounted individually on plastic supports, spatially separated from other individuals, and thread production measured over 24h periods over a range of unidirectional current velocities from 0-45cm . sec-1

NOTE  flow velocities within mussel beds in the field are measured in some cases with “velocimeters” and in others by deploying cylindrical plaster rods at different positions within the beds.  The rate of dissolution of the rods is directly proportional to current flow, and can be easily calibrated (see photograph on Right) 

Research study 9

Some recent work on the molecular and mechanical properties of Mytilus californianus byssus threads comes from researchers at the University of California, Santa Barbara.  The researchers have determined the complete nucleotide sequences of the 3 so-called “preCols” (pre-collagens) making up the threads in M. californianus and have compared them with sequences in the threads of 2 other species M. edulis and M. galloprovincialis, both determined to have mechanically inferior byssus threads.  The thread is made up of 3 “preCols”, the proximal, distal, and NG, the last running the length of the thread (see drawing).  The preCols from M. californianus differ from those of the other 2 species, mainly in being richer in alanine (as is the case with spider silk), thought to enhance strength and stiffness.  In contrast, histidine is rich at schematic drawing of byssus thread of a musselthe terminal ends of all species, suggesting a mechanical role common to all three.  Harrington & Waite 2007 J Exp Biol 210: 4307.

NOTE the NG preCol is not defined by the authors

Morphological and mechanical features of the thread grade from
proximal to distal in accordance with the gradation in collagen
components as shown by the coloured horizontal bars

Research study 10

graph showing tenacities of individual mussels Mytilus californianus on their own and in groups of various sizesOne might think that mussels in a group would be more firmly attached than mussels on their own, but this is not usually the case. Anyone who has collected mussels by hand knows that mussels in layers can often be removed just by reasonably hefty pulling, but individually attached mussels take relatively more effort. Why this is so is explained by researchers at Hopkins Marine Station, California for sea mussels Mytilus californianus. Mussels attach to whatever solid substrata are handy. This means that in a mussel bed photographs of mussels Mytilus californianus to show the difference between intralaminar and interlaminar attachment of byssus threadsconsisting of layers of mussels (for example, two layerst) mussels in the upper layer will attach some threads to other mussels in the same layer ) termed intralaminar, and other threads to mussels in the layer below and also to the substratum (termed interlaminar). In contrast, individual mussels will attach all their threads to the substratum (interlaminar; see photographs on Left). The authors’ study shows that in a bed, many fewer threads are attached interlaminarly (up and down) than intralaminarly (side to side). Thus, when lift is applied to the top layer of mussels, either by wave/current forces or by hand, the layer tends to lift off relatively more easily because there are fewer threads resisting the upward force than are resisting sideways forces. In their comparison of tenacities of individuals with tenacities of groups of 2-6 mussels, the researchers show thaty the latter have tenacities only 57% those of the former (see graph). Although the authors state that “tenacity increases with decreasing group size”, no statistical analysis seems to have been performed on the data and we can only see what appears to be a trend. There is more to the study than presented here, and interested readers are encouraged to give it a go. Cole & Denny 2014 Biol Bull 227 (1): 61.

NOTE these descriptors are workable, but could “primary” for attachment to the substratum and “secondary” for attachment to another mussel be included for better clarity?

NOTE tenacity, or attachment strength, as used here, is the force required to pull a mussel or a group of mussels from its/their attachment using a calibrated spring scale, divided by the mussel(s) “planform” area (cross-sectional area)

  black dot