Marine Mussels. Elizabeth Gosling
Lateral cilia are set along the sides of the filaments in fillibranch gills and in the ostia of eulamellibranch gills. These cilia are responsible for drawing water into the mantle cavity and passing it through the gill filaments or the ostia, and then upward to the exhalant chamber and on to the exhalant opening. Lying between the lateral and frontal cilia (see later) are the large feather‐like latero‐frontal cilia, which are unique to bivalves. When the incoming current hits the gill surface, these cilia flick particles from the water and convey them to the frontal cilia. The frontal cilia, which are abundantly distributed on the free outer surface of the gill facing the incoming current, convey particles aggregated in mucous – secreted by the filaments – downward toward the ciliated food grooves on the ventral side of each lamella. The movement of cilia is under nervous control. Each gill axis is supplied with a branchial nerve from a visceral ganglion, which subdivides to innervate individual groups of filaments. The general architecture and fine structure of the gill vary little from one mussel species to the next, even when rock (e.g. Lithophaga lithophaga; Akşit & Falakali Mutaf 2014) and sediment (e.g. Mytella falcate; David & Fontanetti 2005) burrowing species are considered. See Chapter 4 for a detailed description of the role of the gill in water pumping and particle capture.
In bivalves, the gills have a respiratory as well as a feeding role. Their large surface area and rich haemolymph supply make them well suited for gas exchange. Deoxygenated haemolymph is carried from the kidneys to the gills by way of the afferent gill vein. Each filament receives a small branch of this vein. The filaments are essentially hollow tubes within which the haemolymph circulates. Gas exchange takes place across the thin walls of the filaments. The oxygenated haemolymph from each filament is collected into the efferent gill vein, which goes to the kidney and on to the heart. It is likely that gas exchange also occurs over the general mantle surface.
The gills perform an additional function in hydrothermal vents mussels, which depend almost entirely on endosymbiont chemosynthetic bacteria in the gill filaments as an energy source. The bacteria use the energy obtained from the oxidation of reduced sulphur compounds and methane from hydrothermal fluid for the fixation of the CO2 required for primary production (Duperron et al. 2016 and references therein; see also Chapter 4).
Due to their dominant role in ingestion and respiration, the gills are among the main target organs in the bioaccumulation of pesticides, soluble heavy metals and hydrocarbons. Complex mixtures of heavy metals and polycyclic aromatic hydrocarbons (PAHs) cause morphological changes in the gill epithelium of Mytella falcata, leading to an increase in the number of gill mucous cells, haemocytes and cell turnover processes. These are possible mechanisms to compensate for cell injury and prevent entry of pollutants from gill filaments into the entire organism (David & Fontanetti 2005; David et al. 2008). Exposure to mercury over a 24‐day period caused an initial deterioration in neural and epithelial cells, increased interstitial cell oedema and reduced ciliation in Perna perna. However, after a metal‐free recovery period, gill filament morphology returned to near normal (Gregory et al. 2002). This is not unexpected, as metallothioneins (MTs) – metal‐binding, heat‐stable, low‐molecular‐weight proteins – play an important role in detoxifying trace metals in bivalves and are widely distributed in gill and digestive gland tissue. Consequently, mussel MT levels are increasingly being used as a biomarker of heavy metal contamination in coastal ecosystems (Khati et al. 2012; see Chapter 8).
Foot
The foot first appears when bivalve larvae are about 200 μm in length, and becomes functional in crawling and attachment at ~260 μm shell length. This is the pediveliger stage of development, which immediately precedes settlement and metamorphosis (see Figure 5.10). The ciliated foot is proportionately very large and sock shaped, and is made up of layers of circular and longitudinal muscles surrounding a capacious haemolymph space. A byssal duct opens at the ‘heel’ of the foot, and a byssal pedal groove extends forward along the ‘sole’ from this opening. The groove is embedded in secretory tissue, which produces the different byssal thread components (see later). While swimming, the foot is fully extended, and periodically the velum (larval swimming organ) is withdrawn and the larva sinks to the bottom and begins to crawl. If the substrate is unsuitable (i.e. does not stimulate the secretion of byssus), the foot is withdrawn and the larva once again swims off (Lutz & Kennish 1992). This cycle can be repeated many times over a period of a few days. In Mytilus, when a suitable substrate is found, the larva continues to crawl for some time, gradually ceases movement, protrudes the foot and quickly secretes a single byssal thread. In the newly attached mussel larva, this thread can be repeatedly broken and reformed before final settlement takes place. As the mussel grows in length, more and more attachment threads are secreted; this is not surprising, as larger individuals are subject to greater mechanical stress than smaller ones. To resist dislodgement, mussels cluster their threads in the direction of applied forces (e.g. facing ebb and flow of tide). The adhesive in mussel larvae differs from that of adults, resembling the mucous secreted by other benthic marine species at the larval stage (Petrone et al. 2008). The green crenella, Musculus discors, is unusual in that the byssus threads that are used to fix it to the substrate are woven into a nest or cage surrounding the shell, similar to a ball of twine. Eggs in mucous strings are retained within this nest, which may incorporate a variety of macroalgae (Merrill & Turner 1963).
Byssus Composition
There are four distinct regions in the mussel byssus: root, stem, thread and plaque (Figure 2.9). The root is embedded in the muscular tissue at the base of the foot. The stem is divided into sections, each with a thread attached; each thread ends in a plaque at which attachment to the substrate takes place. In M. edulis and M. galloprovincialis, byssal threads are a few centimetres in length and less than 0.1 mm in diameter (Waite et al. 2002). Each thread is further divided into a smooth and stiff distal region and a soft and wavy proximal region (Figure 2.10A); in terms of mechanical properties, the latter resembles soft rubber (elasticity of 200%) and the former behaves like rigid nylon with a high tensile strength (Young’s modulus = 500 MPa) (Waite et al. 2002). The overall mechanical properties of threads reflect those of elastomers, withstanding significant deformations without rupture and returning to their original state when the stress is removed (Hagenau et al. 2009). Each thread has a flexible, collagenous inner core covered by a tough, durable cuticle (Holten‐Andersen et al. 2009), which has a thickness of 2–5 μm and is composed of the protein mefp‐1, rich in dihydroxyphenylalanine (DOPA) residues. Metal crosslinking of DOPA residues further enhances the toughness of the byssal threads (Arnold et al. 2010). The collagenous proteins that make up the core are known as preCOLs (prepepsinised collagens). The proximal region of the thread contains preCOL‐P, a protein with remarkable extensibility and toughness due to the coiled nature of the collagen fibres (Figure 2.10B). The distal region of the thread contains preCOL‐D, arranged in straight bundles which provide the stiff properties of the thread–plaque interface. A third protein, preCOL‐NG, is distributed throughout the core and is believed to mediate the function between the elastic proximal and stiff distal regions of the thread (Figure 2.11). PreCols extend into the thread–plaque interface. Another component of the core is the thread matrix proteins (TMPs; Figure 2.11), which are distributed throughout the thread and provide a viscoelastic matrix around the collagen fibres (Figure 2.10A). Apparently, TMPs lubricate the fibres and help in reforming byssal threads following deformation from tensile loads (Sagert & Waite 2009). The cuticle, which covers the thread and plaque regions, is about fivefold harder than the thread core. Six different families of