Freshwater Pearl Mussel

If you read Donal Buckley‘s blog, you might notice a lot of physical and biomechanical references. If you read Karen Throsby‘s blog, you’ll notice a lot of sociological analysis of open water and English Channel swimmers in particular. As you go on reading my blog, you might find out more about the zoological and ecological side of swimming. This post is actually an essay that I wrote on one species of freshwater pearl mussel that I’ve become familiar with from swimming in the River Blackwater, though it’s usually empty shells that I come across. I’m sure that most will find this a bit boring but others might find it interesting so here it is anyway (in time, I will get around to writing about some of the more “exciting” species that swimmers encounter):

Margaritifera margaritifera (Linnaeus, 1758)

Introduction

The phylum Mollusca is among the most diverse of the animal phyla in terms of morphology (Passamaneck et al., 2004). Molluscs exhibit a great variety of body forms, but there is one external feature that distinguishes molluscs from other members of the animal kingdom, i.e. the mantle. The mantle encloses many of the vital organs of molluscan organisms and is specialised for a variety of purposes in the various mollusc groups, e.g. cephalopods such as squid use their mantle for jet propulsion (Pörtner, 2002), but the mantle of most molluscs is used for the secretion of a hard, calcareous shell.

Sharma et al. (2012) described the class Bivalvia as the second largest class of the phylum Mollusca. The bivalves are characterised by a laterally compressed body enclosed by two hinged valves (shells) and the lack of the radula-like tongue common in other molluscs (Sharma et al., 2012). This group includes clams, oysters, scallops and mussels and is distributed over a global range.

The subclass Palaeoheterodonta is distinct from other bivalves in that both valves are of the same size and shape and the hinge teeth are arranged in a single row. There are two orders within the paleoheterodonts: Trigonioida (marine) and Unionoida (freshwater). A common family among the unionoids is the family Margaritiferidae. Byrne et al. (2009) found that the most widespread margaritiferid species found in Irish rivers is Margaritifera margaritifera, commonly referred to as the freshwater pearl mussel or “river oyster” in certain areas.

Freshwater pearl mussels (Margaritifera margaritifera) in the Navarån Västernorrland river in Sweden.

Biology: Form & Function

The external morphology of the adult freshwater pearl mussel is similar to that of most other freshwater bivalves. The entire body is enclosed between two kidney-shaped brown or black coloured valves (Degerman et al., 2009). The body is laterally compressed and the posterior end is elongated. The radial depression on the surface of the shell is called the sulcus. Mature specimens can measure 12 cm to 15 cm in length (Skinner et al., 2003) but Degerman et al. (2009) reported that a specimen measuring 17.6 cm was recorded in the county of Jämtland in Sweden.

The valves articulate at a dorsal hinge, which is secured by a ligament. Just ventral to the hinge is the umbo; this is the oldest and thickest part of the valve and growth rings can be seen radiating from it (Nyström et al., 1995). A cross section of a shell reveals three discrete layers; the periostracum, the prismatic layer and the nacreous layer, which lines the internal surface of the shell and is better known as mother-of-pearl (Jacob et al., 2008). The shell is secreted by the epithelial cells of the mantle (Jacob et al., 2008) and serves to protect the mussel’s delicate ctenidia (gills) and other soft body parts from predators and debris moving in the water.

All of the mussel’s soft body parts are located between the two shells and enveloped by the mantle. The mantle’s edge has three distinct pallial lobes; the outer lobe, which secretes the shell, the sensory lobe and the inner lobe, which is muscular. At the posterior end, the inner pallial lobes of the left and right mantles separate to form the incurrent (inhalant) and excurrent (exhalant) siphons. The excurrent siphon is dorsal to the incurrent siphon. Water and food particles are inhaled into the mantle cavity via the incurrent siphon and water and wastes expelled from the mantle cavity via the excurrent siphon (Degerman et al., 2009).

Inside the mantle cavity, a pair of large, feather-shaped ctenidia can be seen extending posteriorly from the visceral mass. The ctenidia of M. margaritifera are specialised for two purposes. The primary function of the ctenidia is to provide a surface for gaseous exchange (Carroll & Catapane, 2007). The respiratory surface area is maximised by a large number of ctenidial plates extending from a central ctenidial axis. The flow of water over the ctenidia is maintained by the movement of cilia on the surface of the ctenidial plates (Carroll & Catapane, 2007). Water flows from the ventral incurrent chamber to the dorsal excurrent chamber, counter to the flow of the blood, thus maximising gaseous exchange. The cilia and grooves on the surface of the ctenidia also play a role in the selection and sorting of food particles from inhaled water (Ward et al., 2003).

Margaritifera margaritifera, like all bivalves, has an open circulatory system. The heart has three chambers (two auricles and one ventricle) and is enclosed by a pericardium. The haemolymph (blood) leaves the heart via a posterior aorta and an anterior aorta. The oxygen-carrying glycoprotein in the haemolymph of M. margaritifera (and most other molluscs) is haemocyanin, and unlike haemoglobin in the erythrocytes of other animals, haemocyanin is suspended freely in the haemolymph (Streit et al., 2005). Gaseous exchange occurs across the ctenidial plates of the gills.

As is the case with other filter-feeding bivalves, M. margaritifera has a complete, though relatively simple, digestive tract. Food particles collected on the gills move proximally towards the mouth, where they are further sorted by the labial palps, before entering the mouth (Ward & Shumway, 2004). M. margaritifera lacks the radula-like tongue characteristic of most molluscs. The mouth and oesophagus are ciliated and serve merely to direct food particles to the stomach (Helm et al., 2004). Mechanical digestion in the stomach is accomplished by a crystalline style, projecting into from an associated sac. This sac is ciliated and the rhythmic motion of the cilia causes the style to rotate, grinding food particles against the gastric shield located on the wall of the stomach (Helm et al., 2004). These food particles then pass to the sorting caecum and enter the digestive diverticula for further digestion. Following digestion, waste products are egested into the excurrent chamber via the anus and are expelled into the water via the excurrent siphon.

The three largest muscle masses of M. margaritifera are the two adductor muscles and the foot. The adductor muscles’ function is to close the shell of the mussel and/or to hold it closed (Itoh et al., 2007). The anterior adductor muscle is located near the mouth, while the posterior adductor muscle is located just posterior to the visceral mass on the dorsal side. The foot of M. margaritifera is recognisable as a large muscular mass projecting anteriorly from the ventral surface of the visceral mass. Its function is to allow the mussel to burrow into the substrate. It achieves this by first extending longitudinally into the substrate, then expanding transversely to form an anchor and finally contracting longitudinally, pulling the entire animal into the substrate (Germann et al., 2011).

Life History & Ecology

Reproductive cycle of the freshwater pearl mussel.

Margaritifera margaritifera is widely known for its longevity. Bauer (1987) found that the main maximum life expectancy of European specimens was 93 ± 9 years. However, it is thought that, given the right conditions, they can live for more than 200 years. One specimen, believed to be as much as 280 years old was found in Sweden (Degerman et al., 2009). The reason for this longevity becomes clear when one considers the reproductive strategy of the mussel.

Margaritifera margaritifera is normally dioecious (Moorkens, 1999) but does not exhibit any external sexual dimorphism (Bauer, 1987). Given certain environmental cues, the male mussel releases sperm aggregates into the water and they are then carried by the water current to the female (Degerman et al., 2009). The fertilised eggs develop on the gills of the female for period of a few weeks before being released into the water as larvae known as glochidia (Skinner et al., 2003). A female can produce several million glochidia each time she reproduces, which can amount to as many as 200 million glochidia if she lives out a normal life span (Bauer, 1987).

Glochidia resemble adult mussels but their shells are open as they drift, suspended in the water column (Skinner et al., 2003). The glochidia are parasitic and must encyst on the gill filaments of a juvenile salmonid fish, e.g. Salmo salar or Salmo trutta, if they are to survive (Skinner et al., 2003). Having survived this stage, the glochidia release from the gills of their host and drop to the riverbed, where they burrow into the substrate and develop for a further 5 years (Moorkens, 1999) before returning to the surface. Mussels reach maturity after about 20 years and once they reach this stage, there is a high probability that they will survive into old age (Bauer, 1987). Bauer (1987) also noted that there is no post-reproductive stage in the life cycle of M. margaritifera, meaning that adults can continue to reproduce into old age.

Margaritifera margaritifera inhabits riverine systems across Eurasia and North America, where it can be found partially buried in the substrate (Skinner et al., 2003). Degerman et al. (2009) described, in detail, the habitat requirements of this species. They point out that populations of M. margaritifera are only known in fast-flowing, clean rivers with stable substrata and where there is a healthy stock of host fish. Skinner et al. (2003) noted that the ideal substratum for this species is coarse sand or fine gravel. They also note that this substratum must be stable and that there should be little or no silt in the interstitial spaces. Shallow water near riffles is favourable as it is more oxygenated and there is less sedimentation.

Hastie & Young (2003) cited Ziuganov et al. (1994) in describing the relationship between M. margaritifera and salmonid fishes as mutually beneficial: the salmonids receive clean water and spawning beds in return for hosting the parasitic glochidia of the mussels. While juvenile mussels may be at risk of predation by fish, adult mussels generally have no natural predators (Degerman et al., 2009).

Margaritifera margaritifera is listed as critically endangered worldwide (IUCN, 2012) and critically endangered in Ireland (Byrne et al., 2009). The widespread and direct exploitation of M. margaritifera for its nacreous pearls and the overfishing of its host fishes have had a long-term effect on the species. More recently, the pollution of rivers and the construction of man-made dams has led to the destruction of much of the mussel’s habitat (Watters, 1995). Extensive conservation projects are underway in Ireland, the UK and across Europe (Skinner et al., 2003).

Freshwater pearl mussel on a German stamp in 2002.

References

• Bauer, G., 1987. Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. Journal of Animal Ecology, 56, 691-704.
• Byrne, A., Moorkens, E.A., Anderson, R., Killeen, I.J. & Regan, E.C., 2009. Ireland Red List No. 2 – Non-Marine Molluscs. National Parks and Wildlife Service, Department of the Environment, Heritage and Local Government, Dublin, Ireland.
• Carroll, M.A., Catapane, E.J., 2007. The nervous system control of lateral ciliary activity of the gill of the bivalve mollusc, Crassostrea virginica. Comparative Biochemistry and Physiology, 148A, 445-450.
• Degerman, E., Alexanderson, S., Bergengren, J., Henrikson, L., Johansson, B.E., Larsen, B.M., Söderberg, H., 2009. Restoration of freshwater pearl mussel streams. WWF Sweden, Solna.
• Germann, D.P, Schatz, W., Hotz, P.E., 2011. Artificial Bivalves – The Biomimetics of Underwater Burrowing. Procedia Computer Science, 7, 169-172.
• Hastie, L.C., Young, M.R., 2003. Conservation of the Freshwater Pearl Mussel: 2. Relationship with Salmonids. Conserving Natura 2000 Rivers, Conservation Techniques Series No. 3, English Nature, Peterborough.
• Helm, H.H., Bourne, N., Lovatelli, A., 2004. Hatchery culture of bivalves. A practical manual. FAO Fisheries Technical Paper, No. 471.
• Itoh, H., Ishii, Y., Watari, T., Tokuda, N., Tsuchiya, T., 2007. Recordings of shell movements and tension changes in vivo in adductor of bivalve. Comparative Biochemistry and Physiology, 148B, 351-352.
• Jacob, D.E., Soldati, A.L., Wirth, R., Huth, J., Wehrmeister, U., Hofmeister, W., 2008. Nanostructure, composition and mechanisms of bivalve shell growth. Geochimicha et Cosmochimicha Acta, 72, 5,401-5,415.
• Moorkens, E.A., 1999. Conservation Management of the Freshwater Pearl Mussel Margaritifera margaritifera. Part 1: Biology of the species and its present situation in Ireland. Irish Wildlife Manuals, No. 8.
• Nyström, J., Lindh, U., Dunca, E., Mutvei, H., 1995. A study of M. margaritifera shells from the River Pauliströmsån, S. Sweden. Nuclear Instruments and Methods in Physics Research, 104B, 612-618.
• Passamaneck, Y., Schander, C., Halanych, K., 2004. Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences. Molecular Phylogenetics and Evolution, 32, 25-38.
• Pörtner, H.O., 2002. Environmental and functional limits to muscular exercise and body size in marine invertebrate athletes. Comparative Biochemistry and Physiology, 133A, 303-321.
• Sharma, P., González, V., Kawauchi G., Andrade, S., Guzmán, A., Collins, T., Glover, E., Harper, E., Healy, J., Mikkelsen, P., Taylor, J., Bieler, R., Giribet, G., 2012. Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca). Molecular Phylogenetics and Evolution, 65, 64-74.
• Skinner, A., Young, M., Hastie, L., 2003. Ecology of the Freshwater Pearl Mussel. Conserving Natura 2000 Rivers, Ecology Series No. 2, English Nature, Peterborough.
• Streit, K., Jackson, D., Degnan, B., Lieb, B., 2005. Developmental expression of two Haliotis asinina hemocyanin isoforms. Differentiation, 73, 341-349.
• Ward, J.E., Levinton, J.S., Shumway, S.E., 2003. Influence of diet on pre-ingestive particle processing in bivalves: I: Transport velocities on the ctenidium. Journal of Experimental Marine Biology and Ecology, 293, 129-149.
• Ward, J.E., Shumway, S.E., 2004. Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. Journal of Experimental Marine Biology and Ecology, 300, 83-130.
• Watters, G.T., 1995. Small dams as barriers to freshwater mussels (Bivalvia, Unionoida) and their hosts. Biological Conservation, 75, 79-85.
• Ziuganov, V., Zotin, A., Nezlin, L., Tretiakov, V., 1994. The Freshwater Pearl Mussels and Their Relationships with Salmonid Fish. VNIRO, Russian Federal Research Institute of Fisheries and Oceanography, Moscow.