Faunal and algal crusts, Echinus esculentus, sparse Alcyonium digitatum and grazing-tolerant fauna on moderately exposed circalittoral rock
Image David Connor - Faunal and algal crusts, Echinus esculentus, sparse Alcyonium digitatum, Abietinaria abietina and other grazing-tolerant fauna on moderately exposed circalittoral rock. Image width ca 1m.
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Ecological and functional relationships
This biotope is dominated by species able to tolerate intense sea-urchin grazing, such as red coralline encrusting algae or rapid growing species which colonize space and grow quickly before they are removed by grazers or predators. The fauna is relatively sparse in comparison to other faunal turf communities (see £CR.Bug£ and £MCR.Flu£), but the epifauna is more developed on vertical surfaces, under overhangs or boulders, in crevices inaccessible to grazing sea urchins and in temporary escapes or predation refuges. Most of the epifauna are sessile, permanently fixed, suspension feeding invertebrates that are, therefore, dependant on water flow to provide: an adequate supply of food and nutrients; gaseous exchange; remove metabolic waste products; prevent accumulation of sediment, and disperse gametes or larvae. Little is known of ecological relationships in circalittoral faunal turf habitats (Hartnoll, 1998) and the following has been inferred from studies of other epifaunal communities (Sebens, 1985; 1986).
Large brown laminarians may be found on the tops of bedrock ridges in the photic zone, giving way to foliose and filamentous red and brown algae (e.g. the red algae Delesseria sanguinea, Cryptopleua ramosa, Lomentaria spp. and Plocamium cartilagineum, and the brown algae Dictyota dichotoma). But large foliose algae are relatively uncommon within the biotope. The dominant macroalgae are grazing tolerant encrusting corallines (e.g. Lithothamnion spp. and Phymatolithon spp.) or non-coralline encrusting algae, which may cover large areas of the rock surface giving it a pink appearance (Sebens, 1985; Hartnoll, 1998; JNCC, 1999).
Active suspension feeders on bacteria, phytoplankton and organic particulates and detritus include sponges (e.g. Pachymastia johnstonia, and Halichondria panicea), the soft coral Alcyonium digitatum, encrusting bryozoans (e.g. Parasmittia trispinosa, Bicellaria ciliata and Crisia eburnea), occasional erect bryozoans (e.g. Bugula species and Flustra foliacea), barnacles (e.g. Balanus crenatus), porcelain crabs (e.g. Pisidia longicornis), and sea squirts (e.g. Ascidia spp., Ascidiella spp., Clavelina lepadiformis, Ciona intestinalis, and Botrylloides leachi). However, the water currents they generate are probably localized so that they are still dependant on water flow to supply adequate food.
Passive suspension feeders on organic particulates, plankton and other small animals include, hydroids (e.g. Abietinaria abietina, Halecium halecium, Kirchenpaueria pinnata and Nemertesia antennina), soft corals (e.g. Alcyonium digitatum), feather stars (e.g. Antedon bifida) and brittlestars (e.g. Ophiothrix fragilis).
Larger prey are taken by passive carnivores such as anemones and cup corals (e.g. Caryophyllia smithii and Urticina felina) (Hartnoll, 1998).
Sea urchins (e.g. Echinus esculentus) are generalist grazers, removing young algae, barnacles, ascidians, hydroids and bryozoans and potentially all epifauna, leaving only encrusting corallines and bedrock. Sea urchins were shown to have an important structuring effect on algal and epifaunal communities and succession (Jones & Kain, 1967; Sebens, 1985; 1986; Hartnoll, 1998) and are no doubt important in this biotope (see seasonal/temporal change below).
Other grazers include top shells (e.g. Gibbula cineraria), small crustaceans (e.g. amphipods) and Calliostoma zizyphinum, which grazes hydroids, while chitons (e.g. Tonicella marmorea) and the tortoise-shell limpet Tectura testudinalis graze encrusting coralline algae.
Specialist predators of hydroids and bryozoans include the nudibranchs (e.g. Doto spp., and Onchidoris spp.) and pycnogonids, (e.g. Nymphon brevirostre), while the nudibranch Tritonia hombergi preys on Alcyonium digitatum, and some polychaetes also take hydroids.
Starfish (e.g. Asterias rubens and Crossaster papposus, Solaster endeca), crabs and lobster are generalist predators feeding on most epifauna, including ascidians and sea urchins
Scavengers include polychaetes, small crustaceans such as amphipods, starfish, brittlestars, and decapods such as hermit crabs (e.g. Pagurus bernhardus) and crabs (e.g. Cancer pagurus and Necora puber).
Mobile fish predators include gobies (e.g. Pomatoschistus spp.), wrasse (e.g. Ctenolabrus rupestris and Labrus bergylta) and butterfish Pholis gunnellus feeding mainly on small crustaceans, while species such as flounder (Platichthys flesus) are generalists feeding on ascidians, bryozoans, polychaetes and crustaceans (Sebens, 1985; Hartnoll, 1998)
Intra and interspecific competition occurs for food and space. Sebens (1985, 1986) demonstrated a successional hierarchy, in which larger, massive, thick growing species (e.g. large anemones, soft corals and colonial ascidians) grew over low lying, or encrusting growth forms such as halichondrine sponges, bryozoans, hydroids and encrusting corallines. In reduced or absent grazing, the epifauna of vertical rock walls became dominated by large massive species, depending on the degree of predation, especially by sea urchins. Sebens (1986) noted that Lithothamnion out-competed Phymatolithon for space, often overgrowing the thinner Phymatolithon. But the thicker, raised and often knobbly Lithothamnion suffered more from sea urchin grazing, so that a competitive equilibrium existed between the two encrusting coralline species in heavily grazed communities (Sebens, 1986).
Seasonal and longer term change
Many of the species within the community demonstrate seasonal changes in abundance and reproduction. Many species of algae show marked seasonal variation in growth with a peak in summer (see Hiscock, 1986c), although in this biotope additional growth merely provides more food for sea urchins. In temperate waters, most bryozoan species tend to grow rapidly in spring and reproduce maximally in late summer, depending on temperature, day length and the availability of phytoplankton (Ryland, 1970). Several species of bryozoans and hydroids demonstrate seasonal cycles of growth in spring/summer and regression (die back) in late autumn/winter, over wintering as dormant stages or juvenile stages (see Ryland, 1976; Gili & Hughes, 1995; Hayward & Ryland, 1998). For example, the fronds of Bugula
species are ephemeral, surviving about 3-4 months but producing two frond generations in summer before dying back in winter, although, the holdfasts are probably perennial (Eggleston, 1972a; Dyrynda & Ryland, 1982). Similarly, Bicellaria ciliata
produces 2 generation per year, larvae from the second generation producing small over wintering colonies (Eggleston, 1972a; Hayward & Ryland, 1998). The uprights of hydroid Nemertesia antennina
die back after 4-5 months and exhibit three generations per year (spring, summer and winter) (see reviews; Hughes, 1977; Hayward & Ryland, 1998; Hartnoll, 1998). Many of the bryozoans and hydroid species are opportunists (e.g. Bugula flabellata
) adapted to rapid growth and reproduction (r
-selected), taking advantage of the spring/summer phytoplankton bloom and more favourable (less stormy) conditions (Dyrynda & Ryland, 1982; Gili & Hughes, 1995). Some species such as the ascidians Ciona intestinalis
and Clavelina lepadiformis
are effectively annual (Hartnoll, 1998). Therefore, the biotope is likely to demonstrate seasonal changes in the abundance or cover of the dominant bryozoans and hydroids. Winter spawning species such as Alcyonium digitatum
may take advantage of the available space for colonization. Seasonal storms probably affect the community removing the uprights of hydroids, erect bryozoans, some ascidians, starfish, sea urchins and mobile epifaunal species, especially where the biotope occurs on boulders or stones that may be mobilized by extreme water movement.
Sebens (1985, 1986) described successional community states in the epifauna of vertical rock walls. Clear space was initially colonized by encrusting corallines, rapidly followed by bryozoans, hydroids, amphipods and tube worm mats, halichondrine sponges, small ascidians (e.g. Dendrodoa carnea and Molgula manhattensis), becoming dominated by the ascidian Aplidium spp., or Metridium senile or Alcyonium digitatum. Sea urchins (e.g. Echinus esculentus in Britain and Ireland) most likely have a significant effect on community structure and succession and their grazing trails can often be seen through bryozoan turfs, leaving bare rock or encrusting corallines behind (Keith Hiscock pers comm.). Sebens (1985, 1986) noted that high levels of sea urchin predation resulted in removal of the majority of the epifauna, leaving encrusting coralline dominated rock. Reduced predation allowed the dominant epifaunal communities to develop, although periodic mortality (through predation or disease) of the dominant species resulted in mixed assemblages or a transition to another assemblage (Sebens, 1985, 1986). Similarly, removal of sea urchins from a 10m wide strip of the Port Erin breakwater allowed macroalgae sporelings, including the kelp Laminaria hyperborea, to colonize the experimental area within a year and only survived within the experimental area (Jones & Kain, 1967). This biotope probably represents an early successional community dominated by encrusting red algae and rapidly colonizing hydroids and tubeworms due to intense grazing pressure. Sebens (1985) noted abrupt changes in the invertebrate communities between horizontal rock faces (as dominate in this biotope) and vertical surfaces and overhangs, which sea urchins find more difficult to traverse. Vertical surfaces and overhangs, and under boulders, exhibited a more developed epifaunal community (Sebens, 1985).
Long term studies of fixed quadrats in epifaunal communities demonstrated that while seasonal and annual changes occurred, subtidal faunal turf communities were relatively stable, becoming more stable with increasing depth and substratum stability (i.e. bedrock and large boulders rather than small rocks) (Osman, 1977; Lundälv, 1985; Hartnoll, 1998). Many of the faunal turf species are long-lived, e.g. 6 -12 years in Flustra foliacea, 5-8 years in Ascidia mentula, over 20 years in Alcyonium digitatum, 8-16 years in Echinus esculentus and probably many hydroids (Stebbing, 1971a; Gili & Hughes, 1995; Hartnoll, 1998). However, Bugula dominated communities recorded from the west Anglesey in 1996 were reported to be 'silted and ragged' in the same season the following year, suggesting some inter-annual variation may occur (Brazier et al., 1999). Lundälv (1985) reported long term stability in presence but short term variation in population density of Ascidia mentula, Ciona intestinalis, Boltenia echinata and Protanthea simplex on rocky sublittoral communities over a 12 year period in the Skagerrak. It was suggested that variations in population density were due to physical disturbance of the communities by storms or grazing by sea urchins, variation decreasing with depth. Sebens (1996) also demonstrated that while epifaunal communities were dominated by the same set of species over a period of years the relative frequency of the different species varied. For example, the sea squirt Aplidium spp. showed a two year cycle of decline and re-growth, consistent with recovery after removal by sea urchin grazing. Therefore, the relative abundance of the epifaunal components of the community are likely to vary with the abundance and long term changes in sea urchin abundance and grazing pressure.
Habitat structure and complexity
This is a rock biotope in which the main habitat complexity is provided by crevices, fissures and overhangs rather than epibiota. Fluctuations in sea urchin grazing will allow rapid colonizing species to develop epifaunal turfs, with occasional escapes of slow colonizing or slow growing species such as sponges and soft corals (e.g. Alcyonium digitatum
), providing some epifaunal complexity in an otherwise sparse community. Well developed epifaunal communities may occur in grazing refuges such as crevices or under hangs.
- The bedrock is dominated by a layer of encrusting corallines, with encrusting bryozoans, and sometimes barnacles e.g. Balanus crenatus
- Where present, encrusting epifauna may be overgrown by erect bryozoans and hydroids (e.g. Bugula species and Nemertesia antennina) interspersed with encrusting sponges, ascidians (e.g. Ascidia spp. ) and Alcyonium digitatum.
- Rock with patches of muddy shell gravel and sand may support Urticina felina (Connor et al., 1997a).
- The faunal crust and sparse turf provides interstices and refuges for a variety of small organisms such as nemerteans, polychaetes, gastropods, and amphipods, while the erect species provide substrata for caprellid amphipods.
- Where present, underboulders and crevices may support the sea cucumber Pawsonia saxicola, squat lobsters (e.g. Galathea spp. and Munida rugosa), encrusting sponges, terebellids, the jingle shell Pododesmus patelliformis (Connor et al., 1997a).
- Fissures and crevices provide shelter for mobile species including decapods crustaceans such as shrimp, crabs and lobsters, sea urchins, starfish and fish. Gobies, wrasse and butterfish probably utilize available rock ledges and crevices, while large species such as flounder and cod probably feed over a wide area, albeit in low numbers.
The biotope may show spatial variation in community complexity and exhibit a mosaic of different species patches (Hartnoll, 1998). For example, with areas recently cleared by predation, disease or physical disturbance in the process of re-colonization, together with areas dominated by Bugula
species, sponges, or ascidians, or areas at intermediate stages of succession. The upper edges or boulders or rocky outcrops, most directly in water flow, tend to exhibit the most species rich and abundant faunal turfs with for example hydroids and perhaps feather stars (e.g. Antedon bifida
). Where sediment scour and abrasion occur (e.g. the sediment/ rock interface), only a small range of species, such as the sponges Polymastia
spp. or the anemone Urticina felina
are able to survive (Stebbing, 1971b, Eggleston, 1972b; Sebens, 1985, 1986; Connor et al.
, 1997a; Hartnoll, 1998; Brazier et al.
Any macroalgae (in shallower examples of this biotope) and encrusting coralline algae provide primary production that enters the food chain indirectly in the form of detritus, algal spores and abraded algal particulates, or directly as food for grazing gastropods, chitons, sea urchins or fish. However, circalittoral faunal turf biotopes are dominated by secondary producers. Food in the form of phytoplankton, zooplankton and organic particulates from the water column together with detritus and abraded macroalgal particulates from shallow water ecosystems are supplied by water currents and converted into faunal biomass. Their secondary production supplies higher trophic levels such as mobile predators (e.g. starfish, sea urchins, and fish) and scavengers (e.g. starfish and crabs) and the wider ecosystem in the form of detritus (e.g. dead bodies and faeces). In addition, reproductive products (sperm, eggs, and larvae) also contribute to the zooplankton (Hartnoll, 1998). However, no estimates of faunal turf productivity were found in the literature.
Most of the species within this biotope produce short-lived, larvae with relatively poor dispersal capacity, resulting in good local recruitment but poor long range dispersal. Most reproductive propagules are probably entrained within the reduced flows within the faunal turf or in turbulent eddies produced by flow over the uneven substratum, resulting in turbulent deposition of propagules locally. Many species are capable of asexual propagation and rapidly colonize space. For example:
- Hydroids are often the first organisms to colonize available space in settlement experiments (Gili & Hughes, 1995). For example, the hydroids Kirchenpaueria pinnata and Abietinaria abietina lack a medusa stage, releasing planula larvae (Cornelius, 1995b). Planula larvae swim or crawl for short periods (e.g. <24hrs) so that dispersal away from the parent colony is probably very limited (Sommer, 1992; Gili & Hughes, 1995). But Nemertesia antennina releases planulae on mucus threads, that increase potential dispersal to 5 -50m, depending on currents and turbulence (Hughes, 1977). Few species of hydroids have specific substrata requirements and many are generalists capable of growing on a variety of substrata. Hydroids are also capable of asexual reproduction and many species produce dormant, resting stages, that are very resistant of environmental perturbation (Gili & Hughes, 1995). Hughes (1977) noted that only a small percentage of the population of Nemertesia antennina in Torbay developed from dormant, regressed hydrorhizae, the majority of the population developing from planulae as three successive generations. Rapid growth, budding and the formation of stolons allows hydroids to colonize space rapidly. Fragmentation may also provide another route for short distance dispersal. However, it has been suggested that rafting on floating debris (or hitch hiking on ships hulls or in ship ballast water) as dormant stages or reproductive adults, together with their potentially long life span, may have allowed hydroids to disperse over a wide area in the long term and explain the near cosmopolitan distributions of many hydroid species (Cornelius, 1992; Gili & Hughes, 1995).
- The brooded, lecithotrophic coronate larvae of many bryozoans (e.g. Flustra foliacea, and Bugula species), have a short pelagic life time of several hours to about 12 hours (Ryland, 1976). Recruitment is dependant on the supply of suitable, stable, hard substrata (Eggleston, 1972b; Ryland, 1976; Dyrynda, 1994). However, even in the presence of available substratum Ryland (1976) noted that significant recruitment in bryozoans only occurred in the proximity of breeding colonies. For example, Hatcher (1998) reported colonization of slabs, suspended 1 m above the sediment, by Bugula fulva within 363 days while Castric-Fey (1974) noted that Bugula turbinata, Bugula plumosa and Bugula calathus did not recruit to settlement plates after ca two years in the subtidal even though present on the surrounding bedrock. Similarly, Keough & Chernoff (1987) noted that Bugula neritina was absent from areas of seagrass bed in Florida even though substantial populations were present <100m away.
- Echinoderms are highly fecund, producing long lived planktonic larvae with high dispersal potential. However, recruitment in echinoderms is poorly understood, often sporadic and variable between locations and dependant on environmental conditions such as temperature, water quality and food availability. For example, in Echinus esculentus recruitment was sporadic and Millport populations showed annual recruitment, whereas few recruits were found in Plymouth populations between 1980-1981 (Nichols, 1984). Bishop & Earll (1984) suggested that the population of Echinus esculentus at St Abbs had a high density and recruited regularly whereas the Skomer population was sparse, ageing and had probably not successfully recruited larvae in the previous 6 years. However, echinoderms such as Echinus esculentus, and Asterias rubens are mobile and widespread and are likely to recruit be migration from other areas.
- Sponges may proliferate both asexually and sexually. A sponge can regenerate from a broken fragment, produce buds either internally or externally or release clusters of cells known as gemmules which develop into a new sponge, depending on species. Most sponges are hermaphroditic but cross-fertilization normally occurs. The process may be oviparous, where there is a mass spawning of gametes through the osculum which enter a neighbouring individual in the inhalant current. Fertilized eggs are discharged into the sea where they develop into a planula larva. However, in the majority development is viviparous, whereby the larva develops within the sponge and is then released. Larvae have a short planktonic life of a few hours to a few weeks, so that dispersal is probably limited and asexual reproduction probably results in clusters of individuals.
- Anthozoans, such as Alcyonium digitatum and Caryophyllia smithii are long lived with potentially highly dispersive pelagic larvae and are relatively widespread. They are not restricted to this biotope and would probably be able to recruit within 2-5 years (refer to the Key Information reviews; Sebens, 1985; Jensen et al., 1994). Juvenile anthozoans are susceptible to predation by sea urchins or overgrowth by ascidians (Sebens, 1985; 1986).
- Ascidians such as Molgula manhattensis, Ciona intestinalis and Clavelina lepadiformis have external fertilization but short lived larvae (swimming for only a few hours), so that dispersal is probably limited (see MarLIN reviews). Where neighbouring populations are present recruitment may be rapid but recruitment from distant populations may take a long time.
- Mobile epifauna will probably recruit from the surrounding area as the community develops and food, niches and refuges become available, either by migration or from planktonic larvae. For example, Hatcher (1998) noted that the number of mobile epifaunal species steady increased over the year following deployment of settlement panels in Poole Harbour.
Recruitment is partly dependant on the availability of free space, provided by grazing, predation, physical disturbance or seasonal die back on some species. The presence of erect species may interfere with recruitment of others, e.g. the dense stands of the hydroid Obelia longissima
inhibited settlement by Balanus crenatus
cyprid larvae but encouraged settlement by ascidian larvae (Standing, 1976). In addition, filter feeding hydroids and anthozoans probably take the larvae of many organisms. Once settled the slow growing species may be overgrown or devoured by predator/grazers, e.g. juvenile Alcyonium digitatum
are highly susceptible to being smothered or eaten when small but can survive intense sea urchin predation when large (Sebens, 1985, 1986). Overall, rapid growth and reproduction secures space in the community for many species e.g. hydroids and bryozoans while ascidians and anthozoans are better competitors but more susceptible to predation (Sebens, 1985; 1986).
Time for community to reach maturity
The recolonization of epifauna on vertical rock walls was investigated by Sebens (1985, 1986). He reported that rapid colonizers such as encrusting corallines, encrusting bryozoans, amphipods and tubeworms colonized within 1-4 months. Ascidians such as Dendrodoa carnea
, Molgula manhattensis
spp. achieved significant cover in less than a year, and, together with Halichondria panicea
, reached pre-clearance levels of cover after 2 years. A few individuals of Alcyonium digitatum
and Metridium senile
colonized within 4 years (Sebens, 1986) and would probably take longer to reach pre-clearance levels.
The addition of sea urchins to vertical rock wall communities previously devoid of urchins resulted in removal of the ascidian Aplidium, the mats of tubiculous amphipods and tubeworms leaving only bare rock within 2-3 months. Only a few large Alcyonium digitatum and fleshy red encrusting algae remained (Sebens, 1985).
Overall a reduction in or absence of sea urchin grazing would allow opportunistic, bryozoans, hydroids, tubeworms and ascidians to grow and colonize space rapidly, probably developing a faunal turf within 1-2 years. Mobile epifauna and infauna will probably colonize rapidly from the surrounding area. However, slow growing species such as some sponges and anemones, will probably take many years to develop significant cover, so that a diverse community may take up to 5 -10 years to develop, depending on local conditions. But on their return, grazing by sea urchins could probably restore the biotope to bare rock dominated by encrusting algae within a few months.
This review can be cited as follows:
Faunal and algal crusts, Echinus esculentus, sparse Alcyonium digitatum and grazing-tolerant fauna on moderately exposed circalittoral 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=337&code=2004>