Bugula spp. and other bryozoans on vertical moderately exposed circalittoral rock
Image Rohan Holt - Bugula spp. and other bryozoans on vertical moderately exposed circalittoral rock Image width ca XX m.
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Ecological and functional relationships
This biotope is dominated by 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).
A few plants are found in this biotope, primarily in the upper reaches of the biotope. 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 reds Delesseria sanguinea, Cryptopleua ramosa, Lomentaria spp. and Plocamium cartilagineum, and the browns Dictyopteris membranacea and Dictyota dichotoma) and eventually articulate corallines and then only encrusting corallines with increasing depth (Sebens, 1985; Hartnoll, 1998; JNCC, 1999).
Active suspension feeders on bacteria, phytoplankton and organic particulates and detritus include sponges (e.g. Pachymastia johnstonia, Clathrina coriacea and Halichondria panicea), the soft coral Alcyonium digitatum, erect and encrusting bryozoans (e.g. Flustra foliacea, Chartella papyracea, Bugula species, Scrupocellaria reptans, Bicellaria ciliata and Crisia eburnea), barnacles (e.g. Balanus crenatus), caprellid amphipods, porcelain crabs (e.g. Pisidia longicornis), and sea squirts (e.g. Aplidium spp., Clavelina lepadiformis 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 carnivores of zooplankton and other small animals include, hydroids (e.g. Tubularia indivisa and Nemertesia antennina), soft corals (e.g. Alcyonium digitatum), while larger prey are taken by anemones and cup corals (e.g. Caryophyllia smithii and Actinothoe sphyrodeta) (Hartnoll, 1998).
Sea urchins (e.g. Echinus esculentus) are generalist grazers, removing 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 epifaunal communities and succession (Sebens, 1985; 1986; Hartnoll, 1998) and are no doubt important in this biotope (see temporal change below).
Other grazers include topshells (e.g. Gibbula cineraria), small crustacea (e.g. amphipods) and Calliostoma zizyphinum, which grazes hydroids.
Specialist predators of hydroids and bryozoans include the nudibranchs (e.g. Doto spp., and Onchidoris spp.) and pycnogonids, (e.g. Achelia echinata), while the nudibranch Tritonia hombergi preys on Alcyonium digitatum, and some polychaetes also take hydroids. Nudibranch life cycles may be closely linked to the life cycles of their prey, and local nudibranchs populations grow rapidly and may denude the hydroid colonies, creating gaps in the epifaunal turf (see Chester et al., 2000).
Starfish (e.g. Asterias rubens and Crossaster papposus), crabs and lobster are generalist predators feeding on most epifauna, including ascidians.
Scavengers include polychaetes, small crustacea such as amphipods, starfish, 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 gunnerellus feeding mainly on small crustacea, 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. Filter feeders reduce the concentration of suspended particulates and deplete food to other colonies/individuals downstream (intra and inter specific competition). Sebens (1985, 1986) demonstrated an 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. The epifauna of vertical rock walls became dominated by large massive species, depending on the degree of predation, especially by sea urchins. However, encrusting bryozoans and encrusting corallines may survive overgrowth (Gordon, 1972; Sebens, 1985; Todd & Turner, 1988).
Seasonal and longer term change
Many of the species within the community demonstrate seasonal changes in abundance and reproduction. 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 hydroid Tubularia indivisa
is annual, dying back in winter (Fish & Fish, 1996), while the uprights of 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 fronds of macroalgae (when present), the uprights of hydroids, 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
. 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).
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 the bryozoan turf, leaving bare rock or encrusting corallines behind (Keith Hiscock pers comm.). The biotope probably represents an intermediate community, in which ascidians and soft corals have not become dominant probably due to predation pressure or competition with erect bryozoans. The similar biotope IR.AlcByH is characterized by a greater abundance of the soft coral Alcyonium digitatum
, possibly representing another stage in the epifaunal succession suggested by 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; 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 of 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).
Habitat structure and complexity
This biotope may occur as part of other faunal biotopes of steep slopes and vertical surfaces. The biotope may occur on steep slopes, vertical surfaces or under overhangs. The species composition probably varies with depth from the lower infralittoral to deep circalittoral. For example, macroalgae probably out compete the faunal turf species on the tops of bedrock ridges but decline on vertical surfaces and with depth. Similarly, Bugula turbinata
tends to dominate in shallower examples, while deeper records have a mixture of Bugula
species dominated by Bugula plumosa
. The different abundance of different Bugula
species is presumably caused by their different preferences for the effects of oscillatory rather than unidirectional water flow (caused by wave action, the effect of which decreases with depth), due to slight differences in colony structure.
- The bedrock is covered by a layer of encrusting corallines, encrusting bryozoans, and sometimes barnacles, especially Balanus crenatus and Verruca stroemia.
- Encrusting epifauna are overgrown by dominant erect bryozoans and hydroids (e.g. Bugula species, Scrupocellaria reptans, Tubularia indivisa and Nemertesia antennina) interspersed with encrusting sponges (e.g. Pachymatisma johnstonia, Haliclona viscosa, Stelligera rigida), ascidians (e.g. Dendrodoa grossularia), Alcyonium digitatum and Urticina felina. The dominance by erect bryozoans and hydroids and ascidians forms a faunal turf over the substratum.
- The faunal 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.
- The erect bryozoans and hydroids support a variety of epizoics that use them as substratum and in some cases affect their growth rates. For example, Bugula flabellata is almost invariably attached to other bryozoans such as Flustra foliacea, while Crisia eburnea grows on macroalgae, hydroids and other bryozoans. Similarly, Alcyonidium parasiticum is epizoic on hydroid stems or the bryozoan Cellaria spp. and the sponge Esperiopsis fucorum may grow on the stem of Tubularia species or on the test of ascidians.
- Mobile species include decapods crustaceans such as shrimp, crabs and lobsters, sea urchins, starfish and fish. Gobies, shannies and butterfish probably utilize available rock ledges and crevices, while large species such as flounder and cod probably feed over a wide area.
- 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, while species richness decreases with proximity to the sediment/ rock interface, which favours species such as the sponges Polymastia spp. or the anemone Urticina felina (Stebbing, 1971b, Eggleston, 1972b; Sebens, 1985, 1986; Connor et al., 1997a; Hartnoll, 1998; Brazier et al., 1999).
- Periodic disturbance of the community due to physical disturbance by storms, extreme scour, or fluctuations in predation, especially by sea urchins, may encourage species richness by preventing dominance by a few species (Osman, 1977; Sebens, 1985, 1986; Hartnoll, 1998).
The presence of macroalgae in the shallower examples of this biotope 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. Although, the biotope occurs within moderately strong to strong water flow that could remove a large proportion of the reproductive output, 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 Aglaophenia plumosa and Sertularia argentea 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). Tubularia indivisa releases a slow crawling actinula larvae with potentially very limited dispersive range (Fish & Fish, 1996). However, 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, Securiflustra securifrons, 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). Actinothoe sphyrodeta is capable of reproducing asexually by fission (Manuel, 1988). Juvenile anthozoans are susceptible to predation by sea urchins or overgrowth by ascidians (Sebens, 1985; 1986). However, recruitment of rare and scarce species, where they occur, such as the sunset cup coralLeptopsammia pruvoti, the Weymouth cup coral Hoplangia durotrix, and the soft coral Alcyonium hibernicum, is likely to take a very long time, e.g. up to 25-30 years or not occur at all in Leptopsammia pruvoti (see MarLIN review).
- Ascidians such as Molgula manhattensis 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 anthozoa 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 recolonized 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.
Jensen et al. (1994) reported the colonization of an artificial reef in Poole Bay, England. They noted that erect bryozoans, including Bugula plumosa, began to appear within 6 months, reaching a peak in the following summer, 12 months after the reef was constructed. Similarly, ascidians colonized within a few months e.g. Aplidium spp. Sponges were slow to establish with only a few species present within 6-12 months but beginning to increase in number after 2 years, while anemones were very slow to colonize with only isolated specimens present after 2 years (Jensen et al., 1994.). In addition Hatcher (1998) reported a diverse mobile epifauna after a years deployment of her settlement panels.
Hydroids are often initial colonizing organisms in settlement experiments and fouling communities (Standing, 1976; Brault & Bourget, 1985; Sebens, 1986; Jensen et al., 1994; Hatcher, 1998). In settlement experiments, the hydroids Cordylophora caspia, Obelia dichotoma and Obelia longissima colonized artificial substrata within ca 1-3 months of deployment (Standing, 1976; Brault & Bourget, 1985: Sandrock et al., 1991). Similarly, Hatcher (1998) reported that Tubularia larynx colonized settlement panels within only 68 days (ca 2 months). Once colonized the hydroids ability to grow rapidly and reproduce asexually is likely to allow them to occupy space and sexually reproduce quickly.
Overall, bryozoans, hydroids, and ascidians are opportunistic, grow and colonize space rapidly and will probably develop 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.
This review can be cited as follows:
Bugula spp. and other bryozoans on vertical 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=105&code=1997>