BIOLOGY OF RIBBED MUSSELS (Geukensia demissa) – With Focus on Jamaica Bay, New York*

Ecology and Life History

Ribbed Mussels are associated with Spartina alterniflora tidal marshes of eastern North America, where they live partially embedded in marsh sediment, or in aggregations of individuals attached by byssal threads to each other and/or to Spartina culms. The mussels are most abundant at lowest shore levels within the marsh, and especially at the lower marsh edge and along creek banks (Kuenzler, 1961,) i.e. at shore levels of 50% of mean high tide or higher. Lent (1967) showed that mussels exposed at low tide are able to exchange gases by "air-gaping." Parrino et al (2000) present evidence that mussels may be able to exploit some energy available from its reduced environment by oxidizing sulphides to synthesize ATP. Mussels tolerate high temperatures but mortality increases at peak temperatures of 45°C and higher (Jost & Helmuth, 2007). The latter research also suggests that the body temperatures of mussels living in marsh grasses may be higher than animals embedded in mud because of reduced convection, in spite shading provided by grasses.

In New York and Southern New England, mussels are found in dense aggregations of 2000-3000 per M^-2 at the marsh edge. Jamaica Bay has higher densities than other estuaries, as high as 10,000 per M^-2 in November (Franz, 2001), and the band of dense mussels is wider. Undoubtedly, high mussel densities are driven, in part, by excessive nitrogen loading and phytoplankton carbon in this system (Benotti, M.J.,et al, 2007), resulting in high chlorophyll-a levels.

Mussels are primarily attached to each other rather than embedded in sediment (Fell et al, 1982; Bertness & Grosholz, 1984; Franz & Tanacredi, 1993; Franz, 1993. Aggregations of mussels also occur at higher shore levels over the entire vertical gradient occupied by Spartina alterniflora, even into the Spartina patens high marsh zone, above MHW (Bertness & Grosholz, 1985; Franz, Unpubl.), although mussel abundance is sharply reduced at higher shore levels.

Feeding Biology

Geukensia demissa is a selective suspension feeder (Espinosa, et al, 2008). In Jamaica Bay, mussel body weights gradually increase beginning in late winter, which suggests that the spring diatom bloom, which occurs locally at this time, contributes to growth and gametogenesis early in the growing season. However, the importance of this linkage can be expected to vary from year to year because in some years intertidal mussels can be frozen under an ice cover in late winter or early spring, which is the time period in which the spring bloom occurs. Summer blooms of nannoplankton, microplankton and bacterioplankton, are characteristic of summer conditions in Jamaica Bay (Peterson & Dam, 1986) and the Hudson Estuary (Malone, 1976.) These organisms have been suggested to be the primary food of Geukensia (Wright et al, 1982; Kemp et al, 1990; Langdon and Newell, 1990.) Recent studies have shown that Geukensia is able to assimilate carbon from bacterioplankton and heterotrophic flagellates (Kreeger & Newell, 1996.) Evidence also shows that while ribbed mussels are able to assimilate lignocellulose from macrophyte detritus, this probably is not a major energy source (Kreeger, Newell & Langdon, 1990.) In Jamaica Bay, summer maxima in both somatic growth (June), shell growth (July-August) and reproductive output (June) of Geukensia demissa are consistent with the hypothesis that mussel production is primarily fueled by summer nannoplankton (Franz, 1997). However, the relative contributions of different nutritional sources will undoubtedly vary among sites. Also, mussels living at the lower marsh edge benefit from diatoms and other sediment-surface micro-organisms which are re-suspended and dispersed into the water column and onto the marsh with each flooding tide (Williams, 1995). Using stable nitrogen isotope ratios, McKinney et al (2001) showed mussel nitrogen isotope signatures are influenced by nitrogen derived from human activities in the watershed adjoining the marsh. Also, Chintala et al (2006) noted a positive correlation between nitrogen loads and mussel biomass and density, which they suggest may reflect increased food resources in highly N-loaded estuaries of the Narragansett Bay system. Clearly this applies to Jamaica Bay, where nitrogen primarily is derived from sewage treatment plants.

Shell Growth

Ribbed mussels can be aged by back counting annual growth lines on the shell (Lutz & Castagna, 1980; Brousseau, 1982.) In Jamaica Bay, new shell growth begins in April and ceases by November. Shell growth rates are highest in July and August (>5 mm per month for 20 mm mussels.) In sexually mature mussels, peaks in body growth rates precede shell growth rate peaks, i.e. body growth and shell growth are "decoupled." (Franz, 1997)

Growth in Relation to Shore Level

Shell growth rates (Kuenzler, 1961;Jordan & Valiella, 1982; Bertness & Grosholz, 1985; Franz & Tanacredi, 1993) and shell length-specific body weights (Franz, 1993) decline significantly with increasing shore level, i.e. mussels of any specific shell length have smaller body weights at higher shore levels than at the marsh edge. (Generally, the marsh edge occurs at about half-tide level (half of the vertical distance between MLW and MHW.) However, when mussel clumps are moved down-shore (e.g. to 25% above MLW), shell and body growth rates are higher than at the marsh edge, as would be expected due to longer submersion times per tidal cycle. Although shell and body growth drops rapidly at shore levels above the marsh edge, fitness losses due to growth reduction may be counterbalanced by increased survivorship and longevity (Bertness, 1980; Bertness & Grosholz, 1985; Stiven & Gardner, 1992, Franz, 2001).

Recruitment and Survivorship

In Jamaica Bay, larvae settle from mid-summer to early fall, primarily on clumps of adult mussels (Nielsen & Franz, 1995.) Bertness & Grosholz (1985) and Nielsen & Franz (1995) have shown that juvenile mussels continue to disperse over short distances (< 1 m) and adjust their positions during the months following settlement. Mortality of larvae while in the plankton is not known.

At the marsh edge in Jamaica Bay, mortality rates of juveniles in the year following settlement averages about 55%, and is particularly sensitive to the severity of winter icing on the marsh (Franz, 2001.) In Jamaica Bay, mussel populations at the marsh edge are composed of 6 or 7 year classes, with decreasing proportions with increasing age. Higher on the shore, the abundance of mussels is much lower than at the edge but additional older age classes are often present, with some mussels reaching 15 years or older. In Jamaica Bay, erosion of the marsh edge is a major source of mussel death. Mussels which fall onto the sand flat at the base of the mussel edge are vulnerable to crab and gull predation, and to burial.

The general absence of mussels below mid-shore levels in Jamaica Bay can probably be explained by two factors: Inability to recover from sediment burial (e.g. after storms); and high rates of predation, by crabs (Callinectes sapidus) and oyster drills (Urosalpinx cinerea and Eupleura caudata). Mussels dislodged from clumps which fall onto the sediment below the marsh edge show little ability to burrow, and do not generally survive.

Reproduction in Relation to Shore Level

Ribbed mussels have separate sexes, In spring and early summer, gonad tubules migrate into the mantle, which becomes thickened. Sex can be determined by the color of the mantle (creamy yellowish-white in males; chocolate brown in females.) Gametogenesis begin in early spring and, in Jamaica Bay, peaks in June and July. It isn't know whether individual mussels spawn more than once during the summer. At the marsh edge, mussels as small as 12 mm are sexually mature, and virtually all mussels > 20 mm are gametogenic during the three months of maximum reproduction (June-August.) However, a few meters upshore from the marsh edge, the minimum size at gametogenesis increases to about 17 mm. Unlike the edge population, it is not unusual for mussels 35 mm or greater in length from higher on the shore to show no external signs of gametogenesis. Between June and August, 1995, 81% of all mussels < 35 mm were gametogenic at the edge as compared to 56.5% at the higher site (Franz, 1996.)

While almost all mussels from the edge population become reproductive in their second year, less than 15% of the higher shore level mussels do so, and even the following year, the frequency of maturation is less than 100%. For the reproductive period June through August, sexual maturation in Geukensia demissa primarily is determined by body weight. At the marsh edge, where submergence times and food abundance are highest, virtually all mussels mature during their second growing season, and some which settle early in the summer may become sexually mature late in their first season. At the higher site, where mussels are food-limited due to shorter feeding times and pre-filtration of tidal flow by mussels living lower on the shore, slower somatic growth rates result in a delay in maturation of one additional year.

Taxonomy and Distribution

Populations of Geukensia demissa (Dillwyn) live predominantly intertidally in salt marshes from the Gulf of St. Lawrence to NE Florida. In estuaries along the Gulf of Maine, Geukensia is scarce, generally absent from salt marshes, and tends to be subtidal.

A subspecies, G. d. granosissima (Sowerby) is distributed from both coasts of Florida to the Gulf of Mexico (Yucatan), predominantly, but not exclusively, in salt marshes. The subspecies differ in shell morphology (rib number) and ultrastructure (Blackwell et al, 1977.) Sarver et al (1992), provide evidence that the southern subspecies should be considered as a separate species.

Although not taxonomically significant, Fields et al (2012) show that based on variation in protein expression, northern populations of G. demissa (New York and north) are physiologically distinct from the southern groups, and that the differences in protein-expression profiles are consistent with greater sensitivity to heat stress to the north.

Importance of Mussels

Previous studies on the ecology of Geukensia demissa have emphasized their ecological roles in affecting nutrient dynamics of the marsh and estuary (Kuenzler, 1961a,b; Jordan and Valiela, 1982), their role in affecting structure of the water-column microbiota (Kemp, Newell & Krambeck, 1990), their interrelationships with the marsh grass Spartina alterniflora , their significance in affecting the physical structure of the marsh (Bertness, 1985), and the effects of shore level, mussel density, and mussel dispersion patterns on mussel growth (Bertness, 1980; Bertness and Grosholz, 1985; Borrero, 1987; Borero and Hilbish, 1988; Lin, 1989; Stiven and Gardner, 1992; Franz, 1993, 1997) or reproductive effort.

It is clear that ribbed mussels are major – if not the dominant - suspension-feeders in Jamaica Bay. The enormous biomass of mussels occurring predominantly along the marsh edge implies that mussels have system-wide ecological effects. If there were to be a large reduction in mussel densities resulting from marsh loss, it could increase phytoplankton abundance, decrease water clarity, and potentially decrease water column DO levels in the Bay (because the quantities of seston currently removed by mussel filtration would remain in the water column).

In the highly eutrophic and nitrogen-loaded Jamaica Bay, managers and others are interested in the possibility that mussels and other bivalves (oysters, hard clams) could contribute significantly to reducing dissolved nitrogen in the Bay. This notion is based on the known capacity of suspension-feeding bivalves to filter large quantities of particulate organic material (phytoplankton & bacterioplankton), some of which are digested and deposited as feces, but most of which are deposited as pseudofeces. Assuming that the pseudofeces remain in the benthic or marsh sediments, organic nitrogen originating from planktonic organisms may be stored as accreting marsh sediment, and some significant portion of this may be removed permanently via microbial denitrifiation.

Nitrogen stored in organic sediment in the marsh may be released into the Bay when marsh sediments erode, a process which is occurring rapidly in Jamaica Bay.

The implication of high and increasing mussel densities for marsh loss remains uncertain. Mussels armor and protect the marsh edge from erosion in the short term, (mussel aggregations are usually the last remnant of the marsh edge to disappear.) Biodeposition rates attributed to feeding processes of ribbed mussels are high, and in some locations may account for most if not all marsh accretion, particularly in summer (Smith & Frey, 1985.) However, it is possible that dense mussel concentrations may also contribute to destabilization of marsh sediments over the longer term. My own studies have shown that biodeposition by mussels is sufficient to produce elevations at the marsh edge (mussel berms) and that pools of standing water may form behind these elevations which do not drain on ebb tide. However, the importance of mussel berms and marsh pools for erosion in the longer term is uncertain. These studies do emphasize the important role of mussels in facilitating biodeposition at the marsh edge. Some of these biosediments wash off the marsh on the ebb tide and are exported back into the Bay, whereas some are retained on the marsh. Whether the marsh interior benefits from increased biodeposition, and whether these materials compensate for possible reduction in natural sediment trapping remain unknown.

Ribbed Mussel References Cited Above

Benotti, M.J., Abbene, Irene., and Terracciano, S.A., 2007, Nutrient Loading in Jamaica Bay, Long Island, New York: Predevelopment to 2005: U.S. Geological Survey Scientific Investigations Report 2007–5051, 17 p, online only.

Bertness, M.D., 1980. Growth and mortality of the ribbed mussel Geukensia demissa (Bivalvia: Dreissenacea). The Veliger 23: 62-69.

Bertness, M.D. and E. Grosholz, 1985. Population dynamics of the ribbed mussel, Geukensia demissa : The costs and benefits of an aggregated distribution. Oecologia 67:192-204.

Blackwell, J.F., L.F. Gainey, Jr. & M. J. Greenbert, 1977. Shell ultrastructure in two subspecies of the ribbed mussel, Geukensia demissa (Dillwyn, 1817) The Biological Bulletin 152: 1-11.

Borrero, F.J. & T.J. Hilbish, 1988. Temporal variation in shell and soft tissue growth of the mussel Geukensia demissa. Marine Ecology Progress Series 42: 9-15.

Brousseau, D.J., 1982. Gametogenesis and spawning in a population of Geukensia demissa (Pelecypoda: Mytilidae) from Westport, Connecticut. The Veliger 24: 247-251.

Castagna, M. and P. Chanley, 1973. Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters of the western Mid- Atlantic coast. Malacologia 12: 47-96.

Chintala, M.M., C. Wigand & G. Thursby, 2006. Comparison of Geukensia demissa populations in Rhode Island fringe marshes with varying nitrogen loads. Marine Ecol. Prog. Ser. 320: 101-108.

Espinosa, E. P., B. Allam and S. E. Ford, 2008. Particle selection in the ribbed mussel Geukensia demissa and the Eastern oyster Crassostrea virginica: Effect of microalgae growth stage. Estuarine, Coastal and Shelf Science 79: 1–6.

Fields, P.A., M.C. Kelly & K.R. Karch, 2012. Latitudinal variation in protein expression after heat stress in the salt marsh mussel Geukensia demissa. Integr. Comp. Biol. 52: 636-647.

Franz, D.R. and J.T. Tanacredi, 1993. Variability in growth and age structure among populations of ribbed mussels Geukensia demissa (Dillwyn)(Bivalvia; Mytilidae), in Jamaica Bay, New York (Gatewaya NRA). The Veliger 36: 220- 227.

Franz, D.R., 1993. Allometry of shell and body weight in relation to shore level in the intertidal bivalve Geukensia demissa (Bivalvia: Mytilidae). Journal Experimental Marine Biology Ecology 174: 193-207.

Franz, D.R., 1996. Size and age at first reproduction of the ribbed mussel Geukensia demissa (Dillwyn) in relation to shore level in a New York salt marsh. Journ. Experimental Marine Biology Ecology 205: 1-13.

Franz, D.R., 1997. Resource alloacation in the intertidal salt-marsh mussel Geukensia demissa in relation to shore level. Estuaries 20: 134-148.

Franz, D.R., 2001. Recruitment, survivorship, and age structure of a New York Ribbed Mussel population (Geukensia demissa) in relation to shore level - a nine year study. Estuaries 24: 319-327

Jordan, T.E. and I. Valiela, 1982. A nitrogen budget of the ribbed mussel, Geukensia demissa, and its significance in nitrogen flow in a New England salt marsh. Limnology and Oceanography 27: 75-90.

Jost, J. and B. Helmuth, 2007. Morphological and ecological determinants of body temperature of Geukensia demissa, the Atlantic ribbed mussel, and their effects on mussel mortality. Biological Bulletin 231(2): 141-151.

Kemp, P.F., S.Y Newall, and C. Krambeck, 1990. Effects of filter-feeding by the ribbed mussel Geukensia demissa on the water-column microbiota of Spartina alterniflora saltmarsh. Marine Ecology Progress Series 50: 119-131.

Kreeger, D.A., R.I.E. Newell and C. J. Langdon, 1990. Effects of tidal exposureon utilization of dietary lignocellulos by the ribbed mussel Geukensia demissa (Dillwyn) (Mollusca: Bivalvia) Journal Experimental Marine Biology Ecology 144: 85-100.

Kreeger, D.A. and R.I.E. Newell, 1996. Ingestion and assimilation of carbon from cellulolytic bacteria and heterotrophic flagellates by the mussels Geukensia demissa and Mytilus edulis (Bivalvia, Mollusca). Aquatic Microbial Ecology 11L 205-214.

Kuenzler, E.J., 1961. Structure and energy flow of a mussel population in a Georgia salt marsh. Limnology and Oceanography 6: 191-204.

Lutz, R.A. and M. Castagna, 1980. Age composition and growth rate of a mussel Geukensia demissa) population in a Virginia salt marsh. Journal Molluscan Studies 46: 106-11

McKinney, R.A., W.G. Nelson, M.A. Charpentier & C. Wigand, 2001. Ribbed Mussel nitrogen isotope signatures reflect nitrogen sources in coastal salt marshes. Ecological Applications 11(1): 203-214.

Nielsen, K.J. and D.R. Franz, 1995. The influence of adult conspecifics and shore level on recruitment of the ribbed mussel Geukensia demissa (Dillwyn) in Jamaica Bay, NY. Journal Experimental Marine Biology Ecology 188: 89-98.

Parrino, V., D.W. Kraus & J.E. Doeller, 2000. ATP Production from the Oxidation of Sulphide in Gill Mitochondria of the Ribbed Mussels Geukensia demissa. Journal of Experimental Biology 23: 2209-2218.

Peterson, W.T. and H.,G. Dam, 1986. Hydrograpy and plankton of Jamaica Bay, New York. Gateway Institute for Natural Resource Science, US-NPS, Gate-N-021-III 21 pp.

Sarver, S.K., M. C. Landrum and D. W. Foltz, 1992, Genetics and taxonomy Marine Biology 113: 385-390.

Smith, J.M. and R.W. Frey, 1985. Biodeposition by the ribbed mussel Geukensia demissa in a salt marsh, Sapelo Island, Georgia. Journal Sedimentary Research 55: 817-828.

Stiven, A.E. and S.A. Gardner, 1992. Population processes in the ribbed mussel Geukensia demissa (Dillwyn) in a North Carolina salt marsh tidal gradient: spatial pattern, predation, growth and mortality. Journal Experimental Marine Biology Ecology 160: 81-102.

West, D.L. and A. H. Williams. 1986. Predation by Callinectes sapidus (Rathbun) within Spartina alterniflora (Loisel) marshes. Journal Experimental Marine Biology Ecology 100: 75-95.

Wright, R.T., R.B. Coffin, C.P. Ersing and D. Pearson, 1982. Field and laboratory measurements of bivalve filtration of natural marine bacterioplankton. Limnology and Oceanography 27 :91-98.

*David R. Franz, Prof. Emeritus of Biology, Brooklyn College CUNY dfranz@brooklyn.cuny.edu; dfranz38@gmail.com