Mytilus edulis and barnacles on very exposed eulittoral rock
Ecological and functional relationships
Rocky shores demonstrate a complex array of ecological relationships, between space occupying species and their predators, and macroalgae and their grazers. The complex of relationships results from variable competitive hierarchies dependant on stochastic events (e.g. larval recruitment, physical disturbance and weather) affecting species abundance and density and deterministic processes such as succession. The information that follows has been derived from survey data (Connor et al., 1997; JNCC, 1999) and more detailed studies by Hawkins & Hartnoll (1983), Suchanek (1985), Tsuchiya & Nishihira (1985 & 1986), Seed & Suchanek (1992), Hawkins et al. (1992), Holt et al. (1998), and Raffaelli & Hawkins (1999). Please note that 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 ecology is probably similar.
Mytilus edulis and Semibalanus balanoides are the dominant space occupying species, competing for available space, Their relative abundance is probably dependant on variation in recruitment intensity and physical disturbance, both species becoming more vulnerable to wave disturbance with age and large size. Mytilus edulis can colonize free substratum but recruitment may be enhanced by the presence of barnacles (Seed & Suchanek, 1992). Mytilus edulis is potentially competitively dominant and capable of overgrowing the barnacles.
Mytilus edulis are active suspension feeders on bacteria, phytoplankton, detritus, and dissolved organic matter (DOM), while barnacles are active and passive suspension feeders on zooplankton and detritus.
The presence of other suspension feeders is probably dependant on the availability of suitable habitats, e.g. interstitial or crevice dwelling micro-molluscs such as Lasaea adansoni and Turtonia minuta or epizoic tubeworms (e.g. Pomatoceros spp.) and the occasional epiphytic hydroid ( e.g. Dynamena pumila).
The macroalgae (e.g. Mastocarpus stellatus, Corallina officinalis, Porphyra umbilicalis and Ceramium spp.) provide primary production to the community and the surrounding ecosystem directly to grazers, or indirectly in the form of abraded algal particulates and detritus, algal spores, algal exudates and dissolved organic matter.
On wave exposed shores, grazers such as limpets and gastropods control macroalgal growth. Limpets are abundant, grazing macroalgal sporelings, benthic microalgae, fucoid fronds and ephemeral seaweeds. Limpet grazing is inhibited by high abundance of older barnacles. Towards the bottom of the shore at the lower limit of the biotope the damper conditions favour macroalgal growth and macroalgal abundance and diversity increases (see Hawkins & Hartnoll, 1983; Hawkins et al., 1992; Raffaelli & Hawkins, 1999). Littorina saxatilis and Littorina neglecta feed on benthic microalgae and sporelings but may switch to fucoids when available (Hawkins & Hartnoll, 1983).
Mesoherbivores such as amphipods and isopods (e.g. Hyale prevosti, Orchestia gammarellus, Idotea granulosa) feeding of ephermeral algae, epiphytic algae, old and dying macroalgae and affect dispersal and recruitment of macroalgal propagules (see Brawley, 1992b).
Patches of mussels support deposit feeders or detritivores such as polychaetes (e.g. Cirratulus cirratus and terebellids) and scavengers feeding on dead mussels within the matrix, e.g. flatworms, small crabs and polychaetes (Kautsky, 1981; Tsuchiya & Nishihira, 1985,1986), while other polychaetes (e.g. scale worms), small crabs and nemerteans are predatory within the matrix.
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. 70mm in length and mussels >45mm 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 starfish (e.g. Asterias rubens), Carcinus maenas and the dogwhelk Nucella lapillus.
Dogwhelks prey on barnacles and mussels, large dogwhelks preferring larger prey (see MarLIN review). The relative importance of dogwhelk predation reduces with increasing wave exposure, except of shores with an adequate supply of refuges (crevices, cracks or gullies) from which dogwhelks can forage (Holt et al., 1998; Raffaelli & Hawkins, 1999).
Flatfish such as Platichthys flesus (plaice), Pleuronectes platessa (flounder) and Limanda limanda (dab), where present, feed on mussels.
Birds are important predators of mussels, and oystercatchers, herring gulls, eider ducks and knot have been reported to be major sources of Mytilus edulis mortality. Although, probably of greatest importance in sedimentary habitats, bird predation, especially by oystercatchers, probably significantly affects the population dynamics of intertidal mussel beds. Oystercatchers and gulls also prey on limpets, while other species of birds probably consume small gastropods, small crustacea (e.g. amphipods and isopods) and crabs.
Seasonal and longer term change
Barnacle dominated rocky shores demonstrate dynamic temporal changes, mediated by relatively random events such as recruitment intensity, and the abundance of grazers and predators. The dynamic changes were best studied in semi-exposed coasts of Isle of Man (Hawkins & Hartnoll, 1983; Hawkins et al.
, 1992; Raffaelli & Hawkins, 1999). In summary, local reductions in limpet abundance result in escapes of fucoids. Clumps of fucoids discourage barnacles settlement due to sweeping of their fronds but encourage recruitment of limpets and dogwhelks which aggregate under their fronds. Fucoids are lost due to wave action, ageing and loss of old barnacles to which they are attached. Fucoids cannot recruit to the available space due to aggregations of limpet. The loss of shelter provided by the fucoids causes limpet and dogwhelks to disperse allowing barnacles to settle. In dense older stands of barnacles limpet graze poorly, allowing escapes of fucoids (see Raffaelli & Hawkins, 1999, figure 4.5). The relative importance of limpet or other gastropod grazing and dogwhelk predation varies with location and shore exposure but is still of importance on exposed shores. The dynamic process favours fucoids on sheltered shores presumably because the macroalgae are able to grow and recruit faster than on exposed shores, whereas wave exposed coasts favour dense barnacles and mussels.
The condition of Mytilus edulis varies with season and reproductive cycle. Spawning is protracted in many populations, with a peak of spawning in spring and summer. A partial spawning in spring is followed by rapid gametogenesis, gonads ripening by early summer, resulting in a less intensive secondary spawning in summer to late August or September. Mantle tissues store nutrient reserves between August and October, ready for gametogenesis in winter when food is scarce. The secondary spawning, is opportunistic, depending on favourable environmental conditions and food availability. Gametogenesis and spawning varies with geographic location, e.g. southern populations often spawn before more northern populations (Seed & Suchanek, 1992).
Winter storms can result in gaps forming in the mussel bed and barnacle cover, especially where the barnacles or mussels are fouled by macroalgae or epifauna, due to wave action and drag, or direct impact by wave driven debris, e.g. logs (Seed & Suchanek, 1992).
Seasonal changes in weather and recruitment will result in variation in the relative abundance of mussel or barnacles, their predators and grazers. For example, hot summers may reduce predation by dogwhelks, grazing by limpets or the upper limit of mussels. Similarly recruitment in Chthamalus
species is favoured in warm years while colder years favour Semibalanus balanoides
(Southward et al.
, 1995; Raffaelli & Hawkins, 1999). Seed (1996) reported that the invertebrate communities within mussel patches exhibit significant temporal and small-scale spatial variations in diversity and abundance, that probably reflect the stochastic nature of larval recruitment and settlement.
The abundance and cover of macroalgae varies with season, fronds dying back or being removed by winter storms to grow back in early spring. Dogwhelk predation pressure varies with season, feeding reduced in winter but active in spring and summer. The barnacle population can be depleted by the foraging activity of the dogwhelk Nucella lapillus
from spring to early winter and replenished by settlement of Semibalanus balanoides
in the spring and Chthamalus
species in the summer and autumn. Crab and fish tend to move to deeper water in the winter months, so that predation is probably reduced in winter.
Habitat structure and complexity
The Mytilus edulis
patches and barnacles dominated substratum denote areas of different habitat complexity and species richness. Patches (or 'islands') of mussels may support a diverse community (see Suchanek,1985; Tsuchiya & Nishihira, 1985, 1986) whereas the interstices of barnacles provide shelter for small species (see Barnes, 2000 for review). Please note that 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 ecology is probably similar. The habitat complexity and species diversity of the shore depends on the relative abundance of mussel and barnacles, the presence of macroalgae and crevices.
Mussel patches ('islands')
Barnacle dominated substratum
- The gaps between interconnected mussels form numerous interstices for a variety of organisms. The interstices between the mussels provide refuge from predation, and provide a humid environment protected from wave action, desiccation, and extremes of temperature. In the intertidal, the species richness and diversity of mussel patches increases with the age and size of the patch (Suchanek, 1985; Tsuchiya & Nishihira, 1985,1986; Seed & Suchanek, 1992). The mussel matrix may support sea cucumbers, anemones, boring clionid sponges, ascidians, crabs, nemerteans, errant polychaetes and flatworms (Suchanek, 1985; Tsuchiya & Nishihira, 1985,1986).
- Mussel faeces and pseudo-faeces, together with silt, build up organic biodeposits under the beds. The biodeposits attract infauna such as sediment dwelling sipunculids, polychaetes and ophiuroids (Suchanek, 1978; Seed & Suchanek, 1992, Tsuchiya & Nishihira, 1985,1986). However, flushing by wave action prevents the build up of the thick layer of biodeposits found in Mytilus reefs.
- Epizoans may use the mussels shells themselves as substrata. However, 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. However, epifauna include barnacles (e.g. Elminius modestus) and tubeworms (e.g. Pomatoceros species)
- Mobile epifauna include isopods, chitons (e.g. Lepidochitona cinerea) and gastropods such as littorinids (e.g. Littorina littorea) and topshells (e.g. Gibbula species), which obtain refuge from predators, especially birds, within the mussel matrix, emerging at high tide to forage (Suchanek, 1985; Seed & Suchanek, 1992).
- The mussels provide a substratum for the attachment of macroalgae such as foliose and filamentous algae e.g. Ceramium species, Palmaria palmata and Porphyra umbilicalis. The abundance of red algae increases down the shore, with Corallina officinalis and Mastocarpus stellatus growing on the substratum. Where macroalgae are present the community also supports small crustaceans such as gammarid amphipods and isopods (e.g. Idotea granulosa) (Seed & Suchanek, 1992, Tsuchiya & Nishihira, 1985,1986). Ephemeral algae such as Ulva spp. and Ulva lactuca may also grow on the mussels themselves.
- Barnacles form a tightly packed covering over the substratum excluding other species. Dead barnacles leave gaps in the covering that can be exploited by small invertebrates.
- Small interstitial species occupy relatively stable microclimates in-between barnacles or in dead barnacles shells, including the small littorinids Littorina neglecta and Littorina saxatilis, the bivalve Lasaea adansoni, intertidal mites, amphipods and isopods.
- Wave sheltered large crevices and gullies provide refuges for dogwhelks and littorinids, while crevices provide refuges for predatory nemerteans and polychaetes (e.g. Eulalia viridis).
The absence, or low abundance, of macroalgae limits primary production in this biotope to microalgae growing on rock surfaces so that primary productivity in the ELR.MytB biotope is probably not as high as some other rocky shore biotopes. Mytilus communities are highly productive secondary producers (Seed & Suchanek, 1992; Holt et al., 1998). Low shore mussels were reported to grow 3.5-4cm in 30 weeks and up to 6-8cm in length in 2 years under favourable conditions, although high shore mussels may only reach 2-3cm in length after 15-20 years (Seed, 1976). However, mussel productivity in this biotope is probably reduced due to their patchy nature. The Mytilus edulis clumps and dense barnacles probably also provide secondary productivity in the form of tissue, faeces and pseudofaeces (Seed & Suchanek, 1992; Holt et al., 1998). Rocky shores can make a contribution to the food of many marine species through the production of planktonic larvae and propagules which contribute to pelagic food chains.
Most species present in the biotope possess a planktonic stage (gamete, spore or larvae) which float in the plankton before settling and metamorphosing into the adult form. This strategy allows species to rapidly colonize new areas that become available such as in the gaps often created by storms. Thus, for organisms such as those present in this biotope, recruitment from the pelagic phase is important in governing the density of populations on the shore (Little & Kitching, 1996). Both the demographic structure of populations and the composition of assemblages may be profoundly affected by variation in recruitment rates.
- Barnacle settlement and recruitment can be highly variable because it is dependent on a suite of environmental and biological factors, such as wind direction and success depends on settlement being followed by a period of favourable weather (see Semibalanus balanoides review for discussion). Long term surveys have produced clear evidence of barnacle populations responding to climatic changes. During warm periods Chthamalus spp. predominate, whilst Semibalanus balanoides does better during colder spells (Hawkins et al., 1994; Southward et al., 1995). Release of Semibalanus balanoides larvae takes place between February and April with peak settlement between April and June. Release of larvae of Chthamalus montagui takes place later in the year, between May and August. However, settlement intensity is variable, subsequent recruitment is inhibited by the sweeping action of macroalgal canopies (e.g. fucoids) or the bulldozing of limpets and other gastropods (see MarLIN review for details).
- Mytilus edulis recruitment is dependant on larval supply and settlement, together with larval and post-settlement mortality. Gametogenesis and spawning varies with geographic location, e.g. southern populations often spawn before more northern populations (Seed & Suchanek, 1992). Spawning is protracted in many populations, with a peak of spawning in spring and summer and settlement approximately 1 month later. JØrgensen (1981) estimated that larvae suffered a daily mortality of 13% in the Isefjord, Denmark. 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. Pedi-veliger larvae may settle first on filamentous substrata, such as hydroids and algae, so that beds of filamentous algae (e.g. Corallina spp., Ceramium spp. and Mastocarpus stellatus) may provide a pool of young mussels that can subsequently colonize the bed. Competition with surrounding adults may suppress growth of the young mussels settling within the mussel bed, due to competition for food and space, until larger mussels are lost (Seed & Suchanek, 1992). However, young mussels tend to divert resources to rapid growth rather than reproduction. 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). 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 spatfall between 1976-1983 in the Exe estuary.
- The Mytilus edulis bed 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. Commito (1987) suggested that species that reproduce with cocoons, brood their young or disperse as juveniles will be favoured (see gastropods below).
- Gastropods exhibit a variety of reproductive life cycles. The common limpet Patella vulgata, the topshell Gibbula umbilicalis, and Littorina littorea have pelagic larvae with a high dispersal potential, although recruitment and settlement is probably variable. Recruitment of Patella vulgata fluctuates from year to year and from place to place. Fertilization is external and the larvae is pelagic for up to two weeks before settling on rock at a shell length of about 0.2mm. Winter breeding occurs only in southern England, in the north of Scotland it breeds in August and in north-east England in September.
However, Littorina obtusata lays its eggs on the fronds of fucoids form which hatch crawl-away miniature adults. Similarly, the dogwhelk Nucella lapillus lays egg capsules on hard substrata in damp places on the shore, from which crawl-aways emerge. Therefore, their dispersal potential is limited but probably designed to colonize an abundant food source. In addition, most gastropods are relatively mobile, so that a large proportion of recruitment of available niches within a mussel bed would involve migration. Nucella lapillus is an exception, as they generally do not move far, averaging 100mm /tidal cycle, or between 30cm or 10m per year when in the vicinity of an abundant food source (see MarLIN reviews for details; Fish & Fish, 1996).
- The propagules of most macroalgae tend to settle near the parent plant (Schiel & Foster, 1986; Norton, 1992; Holt et al., 1997). For example, the propagules of fucales are large and sink readily and red algal spores and gametes and immotile. Norton (1992) noted that algal spore dispersal is probably determined by currents and turbulent deposition (zygotes or spores being thrown against the substratum). For example, spores of Ulva spp. have been reported to travel 35km, Phycodrys rubens 5km and Sargassum muticum up to 1km, although most Sargassum muticum spores settle within 2m. The reach of the furthest propagule and useful dispersal range are not the same thing and recruitment usually occurs on a local scale, typically within 10m of the parent plant (Norton, 1992). Vadas et al. (1992) noted that post-settlement mortality of algal propagules and early germlings was high, primarily due to grazing, canopy and turf effects, water movement and desiccation (in the intertidal) and concluded that algal recruitment was highly variable and sporadic. However, macroalgae are highly fecund and widespread in the coastal zone so that recruitment may be still be rapid, especially in the rapid growing ephemeral species such as Ulva spp. and Ulva lactuca, which reproduce throughout the year with a peak in summer. Similarly, Ceramium species produce reproductive propagules throughout the year, while Mastocarpus stellatusproduce propagules form February to December, and exhibit distinct reproductive papillae in summer (Dixon & Irvine, 1977; Burrows, 1991; Maggs & Hommersand, 1993).
- Many species of mobile epifauna, such as polychaetes have long lived pelagic larvae and/or are highly motile as adults. Gammarid amphipods brood their embryos and offspring but are highly mobile as adults and probably capable of colonizing new habitats from the surrounding area (e.g. see Hyale prevosti review).
Time for community to reach maturity
Bennell (1981) observed that barnacles that were removed when the surface rock was scraped off in a barge accident at Amlwch, North Wales returned to pre-accident levels within 3 years. However, barnacle recruitment can be very variable because it is dependent on a suite of environmental and biological factors, such as wind direction, so populations may take longer to recruit to suitable areas. Recolonization of Patella vulgata
on rocky shores is rapid as seen by the appearance of limpet spat 6 months after the Torrey Canyon
oil spill reaching peak numbers 4-5 years after the spill (Southward & Southward, 1978). Larval supply and settlement in Mytilus edulis
could potentially occur annually, however, settlement is sporadic with unpredictable pulses of recruitment (Lutz & Kennish, 1992; Seed & Suchanek, 1992). Therefore, while good annual recruitment is possible, recovery of the mussel population may take up to 5 years. In certain circumstances and under some environmental conditions recovery may take significantly longer (Seed & Suchanek, 1992).
Tsuchiya & Nishihira (1986) examined young and older patches of Mytilus edulis in Japan, now thought to be Mytilus galloprovincialis (Seed, 1992).. 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. Tsuchiya & Nishihira (1986) did not suggest a timescale. Colonization of the community associated with the mussel patches is therefore, 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.
Recovery of the rocky shore populations has been intensively studied after the Torrey Canyon
oil spill in March 1967. Areas affected by oil alone recovered rapidly, within 3 years. But other sites suffered substantial damage due to the spilled oil and the application of aromatic hydrocarbon based dispersants. Populations of fucoids were abnormal for the first 11 years, and Patella vulgata
populations were abnormal for at least 10-13 years. Recovery rates were dependant on local variation in recruitment and mortality so that sites varied in recovery rates, for example maximum cover of fucoids occurred within 1-3 years, barnacle abundance increased in 1-7 years, limpet number were still reduced after 6-8 years and species richness was regained in 2 to >10 years. Overall, recovery took 5-8 years on many shores but was estimated to take about 15 years on the worst affected shores (Southward & Southward, 1978; Hawkins & Southward, 1992; Raffaelli & Hawkins, 1999).
This review can be cited as follows:
Mytilus edulis and barnacles on very exposed eulittoral rock.
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=203&code=1997>