Mytilus edulis and piddocks on eulittoral firm clay
Ecological and functional relationships
Filter / suspension feeding organisms such as the piddocks Barnea candida, Petricola pholadiformis and Pholas dactylus, the mussel Mytilus edulis and the sand mason worm Lanice conchilega, are the dominant trophic group in the biotope. They feed on phytoplankton and detritus but also small zooplankton and dissolved organic material. Other associated suspension feeders may include the barnacles Semibalanus balanoides and Elminius modestus, mud shrimps Corophium spp. and the slipper limpet Crepidula fornicata. Inter and intra-specific competition for food may exist between the key structural species (see Species Composition) and other filter feeders within the biotope.
The common shore crab Carcinus maenas is the predominant mobile species in the biotope, travelling through as it scavenges for food. It is a significant predator on both adult mussels and their spat.
The algae that occur in small loose lying patches or attached to cobbles on the surface of the clay may provide shelter and possibly a source of food for the grazing prosobranchs Littorina littorea, which frequently occurs in the biotope. Littorina littorea feed within and around the mussel bed, grazing on benthic microalgae and macroalgae (sporeling and adult plants), and bulldozing newly settled invertebrate larvae (Hawkins & Hartnoll, 1983).
Predation is the single most important source of mortality in Mytilus edulis populations (Seed & Suchanek, 1992; Holt et al., 1998). Many predators target specific sizes of mussels and, therefore influence population size structure. For example, Carcinus maenas was unable to consume mussels of ca. 70 mm in length and mussels >45 mm long were probably safe from attack (Davies et al., 1980; Holt et al., 1998).
The lower limit of intertidal mussel populations may be limited by predation by Carcinus maenas.
Birds are important predators of mussels. Oystercatchers, herring gulls, eider ducks and knot have been reported to be major sources of Mytilus edulis mortality. For example, in the Ythan estuary bird predation consumed 72% of mussel production, with oystercatchers and herring gulls being each responsible for 15%. Mussels are regarded as a staple food of oystercatchers (Dare, 1976; Holt et al., 1998). It is not known if birds are significant predators of the piddock species but the areas in which this biotope is found are often important sites for thousands of wildfowl and wading birds.
Seasonal and longer term change
- It is unlikely that piddock populations will be subject to significant seasonal changes in abundance. Petricola pholadiformis, for example, has a longevity of up to 10 years (Duval, 1963a) and its established populations may not exhibit significant seasonal changes, besides spawning in the summer. Pholas dactylus live to approximately 14 years of age, and spawning usually occurs between May and September with settlement and recruitment of juvenile piddocks occuring between November and February (Pinn et al., 2005).
- Mytilus edulis spawns in spring and summer and in some areas again in August and September, with settlement occurring 1-4 weeks later. However, while recruitment can be annual, it is often sporadic and unpredictable. The species richness of the macro-invertebrate fauna associated with mussel patches was shown to fluctuate seasonally, probably reflecting random fluctuations in settlement and mortality typical of marine species with planktonic larvae (see Seed, 1996 for discussion). Winter storms can remove clumps of mussels, especially where the mussels are fouling by macroalgae or epifauna, due to wave action and drag, or direct impact by wave driven debris, e.g. logs (Seed & Suchanek, 1992).
- The Carcinus maenas population may migrate offshore in the winter, therefore reducing predation pressure on the mussels.
- Macroalgae populations are also likely to exhibit some seasonal differences with a general decline in abundance / biomass over the winter months.
Habitat structure and complexity
Clay platforms can support rich and diverse communities. Piddock burrowing creates a generally uneven surface on a small scale (5-15 cm) providing habitats for other animals that inhabit vacant burrows and crevices in the clay. Resident piddock populations can result in extensively burrowed clay and empty piddock burrows can influence the abundance of other species by providing additional habitats and refuges (Pinn et al.
, in press). Wallace & Wallace (1983) reported densities of 30-60 Barnea candida
siphon holes per square foot in Merseyside and burrows up to 6 inches deep. Duval (1977) found that the depth of the boring depended on the size of the animal. For example, an animal with a shell length of 1.2 cm could bore a 2.7 cm burrow whereas animals 4.8 cm long could bore burrows of 12 cm. Pinn et al.
(in press) found a statistically significant increase in species diversity in areas where old piddock burrows were present compared to where they were absent. Empty shells protruding from the eroded surface are also an important settlement surface within this habitat. Due to the impervious nature of the clay, small depressions on the surface can retain water as the tide goes out. In the Swale, Kent, these areas of shallow water have been colonized by the suspension feeders Crepidula fornicata
and Hydrallmania falcata
and the red algae Halurus flosculosus
(as Griffithsia flosculosa
) and Dictyota dichotoma
(Hill et al
Mussel beds can be divided into three distinct habitat components: the interstices within the mussel matrix; the biodeposits beneath the bed; and the substratum afforded by the mussel shells themselves (Suchanek, 1985; Seed & Suchanek, 1992). The sediments, shell fragments and byssal threads that form important components of the mussel patches are important for increasing the heterogeneity of the environments (Tsuchiya & Nishihira, 1986). After the settlement of mussel larvae, a monolayer is formed in the early stages of patch growth (Tsuchiya & Nishihira, 1986). As the patch grows, and the mussels require more space, mussels on the outside may be pushed outwards whilst those on the inside may be pushed up, resulting in the formation of a multi-layered mussel bed (Tsuchiya & Nishihira, 1986). If surface space is limited, as is likely if the sediment surface is extensively bored by the piddocks, mussels may be forced upwards rather than outwards in their patches. This will result in further increases to the heterogeneity of the substratum. Recent evidence suggests that the Mytilus edulis communities studied by Suchanek 1985 and Tsuchiya & Nishihira (1985, 1986) were probably Mytilus trossulus and Mytilus galloprovincialis respectively (Seed, 1992), although their community structure is probably similar to that of Mytilus edulis.
- The interstices between the mussels provide refuge from predation, and a humid environment protected from wave action, desiccation, and extremes of temperature.
- In the intertidal, Mytilus sp. Beds the species richness and diversity increases with the age and size of the bed (Suchanek, 1985; Tsuchiya & Nishihira, 1985,1986; Seed & Suchanek, 1992). However, the biotope is characterized by small clumps of mussels.
- Mussel faeces and pseudo-faeces, together with silt, build up organic biodeposits under the patches. In mussel beds the silt supports infauna such as sediment dwelling sipunculids, polychaetes and ophiuroids (Suchanek, 1978; Tsuchiya & Nishihira, 1985,1986; Seed & Suchanek, 1992).
- Mytilus edulis can use its prehensile foot to clean fouling organisms from its shell (Theisen, 1972). Therefore, the epizoan flora and fauna is probably less developed or diverse than found in beds of other mussel species but may include barnacles (e.g. Elminius modestus) and tubeworms (e.g. Pomatoceros species)
- Mobile epifauna including Littorina littorea can obtain refuge from predators, especially birds, within the mussel matrix and emerge at high tide to forage (Suchanek, 1985; Seed & Suchanek, 1992).
- The mussels provide a substratum for the attachment of foliose and filamentous algae e.g. Ceramium species, Mastocarpus stellatus and Ulva lactuca. These algae in turn can provide a habitat for cryptic fauna such as amphipods.
- Piddocks increase the structural complexity of the habitat through their burrowing activities, which results in an increase in species diversity (Pinn et al., in press).
Dense beds of bivalve suspension feeders increase turnover of nutrients and organic carbon in estuarine (and presumably coastal) environments by effectively transferring pelagic phytoplanktonic primary production to secondary production (pelagic-benthic coupling) (Dame, 1996).
- Specific information about the productivity of the key structural species was not found. However, the piddocks together with the mussels mean that detritus will contribute the most to the productivity of the biotope.
- Mytilus spp. Communities are highly productive secondary producers (Seed & Suchanek, 1992; Holt et al., 1998). Low shore mussels were reported to grow 3.5-4 cm in 30 weeks and up to 6-8 cm in length in 2 years under favourable conditions, although high shore mussels may only reach 2-3 cm in length after 15-20 years (Seed, 1976). Seed & Suchanek (1992) suggested that in populations of older mussels, productivity may be in the region of 2000-14,500 kJ/m²/yr. However, this biotope is characterized by patches of mussels, as opposed to mussel beds, and although mussel productivity is nevertheless important, it will not be as high as productivity from mussel beds. In Killary Harbour, western Ireland, the shore population of mussels contributed significantly to the larval population of the inlet. Kautsky (1981) reported that the release of mussel eggs and larvae from subtidal beds in the Baltic Sea contributed an annual input of 600 tons of organic carbon/yr. to the pelagic system. The eggs and larvae were probably an important food source for herring larvae and other zooplankton. The Mytilus edulis beds probably also provide secondary productivity in the form of tissue, faeces and pseudofaeces (Seed & Suchanek, 1992; Holt et al., 1998). Maximum growth rates for the piddocks Pholas dactylus, Barnea candida and Barnea parva were found to be respectively about 7 mm, 10 mm and 4 mm per growth line.
- The small amount of macroalgae associated with this biotope including Mastocarpus stellatus, Ceramium species and Ulva intestinalis will contribute some dissolved organic carbon to the biotope. This is taken up readily by bacteria and may even be taken up directly by some larger invertebrates. Only about 10% of the primary production is directly cropped by herbivores (Raffaelli & Hawkins, 1996). Dissolved organic carbon, algal fragments and microbial film organisms are continually removed by the sea. This may enter the food chain of local, subtidal ecosystems, or be exported further offshore. Measurements of the productivity of benthic algae are relatively few, particularly for the Rhodophyta (Dixon, 1973). Blinks (1955) estimated the net production of red algae to be in the order of 11 to 54 g dry weight per m² per day.
Most of the characterizing species in the biotope are sessile or sedentary suspension feeders. Recruitment of adults of these species to the biotope by immigration is therefore unlikely. Consequently, recruitment occurs primarily through dispersive larval stages. However, recruitment in many bivalve species is sporadic with unpredictable recruitment episodes.
- The three piddock species Pholas dactylus, Petricola pholadiformis and Barnea candida spawn in the summer months of July, August and September respectively. Settlement and recruitment of juvenile piddocks into the population is known to occur over an extended period between the months of November and February (Pinn et al., 2005). El-Maghraby (1955) showed that in southern England Barnea candida was unusual in that it started to spawn when the temperature fell at the beginning of the autumn (September).
- The fecundity of female Petricola pholadiformis is estimated to be between 3 - 3.5 million eggs per year (Duval, 1963a).
- Mytilus edulis recruitment is dependant on larval supply and settlement, together with larval and post-settlement mortality. Jørgensen (1981) estimated that larvae suffered a daily mortality of 13% in the Isefjord, Denmark but Lutz & Kennish (1992) suggested that larval mortality was approximately 99%. Larval mortality is probably due to adverse environmental conditions, especially temperature, inadequate food supply (fluctuations in phytoplankton populations), inhalation by suspension feeding adult mytilids, difficulty in finding suitable substrata and predation (Lutz & Kennish, 1992). Widdows (1991) suggested that any environmental factor that increased development time, or the time between fertilization and settlement would increase larval mortality.
- Recruitment in many Mytilus sp. populations is sporadic, with unpredictable pulses of recruitment (Seed & Suchanek, 1992). Mytilus sp. is highly gregarious and final settlement often occurs around or in-between individual mussels of established populations. Persistent mussels beds can be maintained by relatively low levels of recruitment e.g. McGrorty et al., (1990) reported that adult populations were largely unaffected by large variations in spat fall between 1976-1983 in the Exe estuary.
- The Mytilus edulis patch may act as a refuge for larvae or juveniles, however, the intense suspension feeding activity of the mussels is likely to consume large numbers of pelagic larvae.
- Littorina littorea can breed all through the year although the length and timing of the breeding period is dependent on climatic conditions. Large females can produce up to 100, 000 eggs during this time. The pelagic phase of the larvae can be as long as six weeks providing potential for dispersal.
- The breeding season in Carcinus maenas depends on geographic location and in general, the length of the breeding period increases further south in England with year round breeding possible on the south coast. Fecundity in females can exceed 100, 000 eggs.
Time for community to reach maturity
Little information was found concerning community development. However, piddocks, Barnea candida
, Pholas dactylus
and Petricola pholadiformis
are likely to settle readily. These piddocks breed annually and produce a large number of gametes. Once established individuals may live for a considerable length of time; Petricola pholadiformis
of length 5-6 cm are likely to be between 6-10 years old (Duval, 1963a). Pinn et al.
(2005) estimated the maximum age of Pholas dactylus
, Barnea candida
and Barnea parva
to be 14 years, 4 years and 6 years respectively. Duval (1977) proposed that it was as a result of the extensive borings of Barnea candida
that facilitated the colonization of an area in the Thames Estuary by the introduced American piddock, Petricola pholadiformis
. This suggests that Barnea candida
is a more competitive colonizing species in clay environments than the American piddock and it is possible that this species will appear first on cleared substrates.
Mytilus spp. populations are considered to have a strong ability to recover from environmental disturbance (Seed & Suchanek, 1992; Holt et al., 1998). Larval supply and settlement could potentially occur annually, however, settlement is sporadic with unpredictable pulses of recruitment (Lutz & Kennish, 1992; Seed & Suchanek, 1992). The presence of macroalgae in disturbance gaps in Mytilus califorianus populations, where grazers were excluded, inhibited recovery by the mussels. In New England, U.S.A, prior barnacle cover was found to enhance recovery by Mytilus edulis (Seed & Suchanek, 1992). While good annual recruitment is possible, recovery of the mussel population may take up to 5 years. However, recovery of the mussel population may be delayed by 1-7 years for the initial macroalgal cover to reduce and barnacle cover to increase. Therefore, the biotope may take between 5 -10 years to recover depending on local conditions. Once the patches of mussels have returned, colonization of the associated community is dependant on the development of a mussel matrix, younger beds exhibiting lower species richness and species diversity than older beds, and hence growth rates and local environmental conditions. Tsuchiya & Nishihira (1986) examined young and older patches of Mytilus (probably Mytilus galloprovincialis) in Japan. They noted that as the patches of mussels grew older, individuals increased in size, and other layers were added, increasing the space within the matrix for colonization, which also accumulated biogenic sediment. Increased space and organic sediment was then colonized by infauna and epiphytes and as the patches and mussels became older, eventually epizoic species colonized the mussel shells. Macroalgae could colonize at any time in the succession. Unfortunately, Tsuchiya & Nishihira (1986) did not suggest a timescale.
This review can be cited as follows:
Mytilus edulis and piddocks on eulittoral firm clay.
Marine Life Information Network: Biology and Sensitivity Key Information Sub-programme [on-line].
Plymouth: Marine Biological Association of the United Kingdom.
Available from: <http://www.marlin.ac.uk/habitatecology.php?habitatid=95&code=2004>