Grazed Laminaria hyperborea with coralline crusts on infralittoral rock
Image Keith Hiscock - Grazed Laminaria hyperborea forest with coralline crusts on upper infralittoral rock (MIR.LhypGz.Ft). Image width ca 2 m.
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Ecological and functional relationships
Kelps are major primary producers. Up to 90% of kelp production enters the detrital food web and kelp is probably a major contributor of organic carbon to surrounding communities (Birkett et al., 1998b). Kelp beds are diverse species rich habitats and over 1,800 species have been recorded in the UK kelp biotopes (Birkett et al., 1998b). Kelp communities and the interaction between kelp, urchins and predators has been studied in Nova Scotia, Norway, southern California and the UK (Kain, 1979; Mann, 1982; Schiel & Foster, 1986; Elner & Vadas, 1990; Vadas & Elner, 1992; Sivertsen, 1997). The following are important ecological relationships.
Sea-urchins graze rock surfaces including juvenile kelp sporophytes, together with epiphytes and epifauna on laminarian stipes. It is sea urchin grazing that gives the rocks their bare appearance below the kelp. Grazing may prevent potentially dominant species from becoming established and therefore facilitate species richness. Vost (1983) examined the effect of removing grazing Echinus esculentus and found that after 6-10 months the patchiness of the understorey algae had decreased and the species richness and biomass of epilithic species increased. Strongylocentrotus droebachiensis and Paracentrotus lividus also graze kelp beds but are less common in the British Isles than Echinus esculentus. Echinus esculentus grazing probably controls the lower limit of Laminaria hyperborea distribution in some locations, e.g. in the Isle of Man (Jones & Kain, 1967; Kain et al., 1975; Kain, 1979).
Epifauna is more developed on vertical surfaces, under overhangs or boulders and in crevices inaccessible to grazing sea urchins.
Helcion pellucidum grazes epiphytes and the kelp tissue directly, forming pits similar to the home scars of intertidal limpets (see Kain & Svendsen, 1969 for photographs). The larger, Helcion pellucidum laevis form excavates large cavities in laminarian holdfasts. This tissue damage weakens the adult plant and contributes to its loss due to wave action and storms (Kain, 1979, Birkett et al., 1998b). Infestation with Helcion pellucidum varies between sites and decreases with depth, e.g. infestation may reach up to 50 % on mature plants in shallow water in the Isle of Man, whereas <20 % was found (on kelps of any age group and depth) in England and Scotland (Kain, 1979).
Laminaria hyperborea is grazed directly by Lacuna vincta in Norway, the individuals forming deep pits in the lamina (Kain, 1979).
Kelp fronds, stipes and holdfasts provide substrata for distinct communities of species, some of which are found only or especially on kelp plants. Kelp holdfasts provide both substrata and refugia (see Habitat complexity).
Epiphytes and understorey algae are grazed by a variety of amphipods, isopods and gastropods, e.g. Littorina spp., Acmaea spp., Haliotis tuberculata, Aplysia spp. and rissoid gastropods (Birkett et al., 1998b).
Predators within kelp beds have not been well studied in the UK. Lobsters (e.g. Homarus gammarus), crabs and some fish species (e.g. the wolf fish Anarhichas lupus) and perhaps otters are known to consume gastropod and echinoderm grazers.
Birkett et al. (1998b) suggest that juveniles of animals present in kelp beds as adults probably use the habitat as a nursery and unknown numbers of species are likely to use the habitat during their life cycle. Rinde et al. (1992, cited in Birkett et al., 1998b) state that Norwegian kelp beds are nurseries for gadoid species.
Seasonal and longer term change
The most conspicuous changes are likely to be in the abundance of algae and of associated species such as encrusting Bryozoa in the biotope. New blades of Laminaria hyperborea
grow in winter between the meristem and the old blade, which is shed in early spring or summer together with associated species growing on its surface. Larger and older kelp plants become liable to removal by wave action and storms due to their size and weakening by grazers such as Helcion pellucidum
. There is therefore likely to be a reduced abundance of kelps following the winter. Red algae show significant variability in abundance through the year with fresh growths appearing in spring, growing rapidly and being degraded by herbivores and by growths of animals such as hydroids and encrusting Bryozoa through the summer. Hiscock (1986c) demonstrated significant changes in red algae on pebble communities and it is likely that similar changes occur on bedrock.
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 uprights of the hydroid Nemertesia antennina die back after 4-5 months and exhibit three generations per year (spring, summer and winter) (see MarLIN reviews; Hughes, 1977; Hartnoll, 1998; Hayward & Ryland, 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.
Some species may vary in abundance from year-to-year for no apparent reason. For instance, the sea squirt Clavelina lepadiformis
may be abundant in some years but not others (Hiscock, 1994). Other species may lose condition or otherwise change in appearance. For instance, from February through to July colonies of the soft coral Alcyonium digitatum
expand and feed regularly. However, from late July through to December colonies remain contracted, during which time they do not feed and assume a shrunken appearance and become colonized by hydroids, algae and tube amphipods (Hartnoll, 1985). Fish populations that inhabit the biotope (especially wrasse, pollock and gobies) may show seasonal changes that reflect migration to deeper and therefore calmer water in winter and possibly mortality following adverse autumn conditions.
Habitat structure and complexity
Habitat complexity is the result of both substratum architecture and the organisms that characterize this biotope. Rock surfaces may be smooth or broken and may include fissures, crevices and, where composed of boulders, refugia for a wide range of mobile and sessile species under the boulders. Species such as squat lobsters, Galathea
spp., may be present in fissures emerging only at night whilst sea cucumbers such as Pawsonia saxicola
and brittle stars such as Ophiopholis aculeata
may live in crevices with only feeding arms protruding.
Kelp plants themselves provides a variety of habitats and refugia in a similar way to terrestrial forests. Kelps also reduce current flow and their canopy shades the understorey vegetation and substrata producing a particular microclimate depending on the depth and density of the kelp plants. In kelp forest (e.g. EIR.LhypR.Ft) the kelp density produces a canopy which excludes up to 90% of incident light encouraging the presence of shade tolerant algae, mainly reds and animals to occur where they can escape grazing. In deeper water, as light intensity decreases, the kelp density decreases forming a kelp park. Kelp beds are patchy and dynamic with areas devoid of kelp (due to storms, wave surge or grazing) in the process of expansion or recolonization in different stages of succession. Species diversity changes with depth, between forest & park, with exposure, substratum and turbidity (Norton et al. 1977; Erwin et al. 1990; Birkett et al. 1998b). Erwin et al. (1990) noted that species richness increased in the kelp park (as lower infralittoral and upper circalittoral species overlapped) and was higher in boulder fields in which sand-scour and substratum heterogeneity provided more niches for colonization. Kelp beds exhibit a series of stratified habitats, and a patchwork of species depending on the substratum, light, water flow and exposure.
- Planktonic: Spores and larvae from algae and benthic organisms within the bed, as well as from the surrounding area, probably form an import food source given the number of suspension feeding organisms in kelp beds
- Nekton: wrasse and pollock have been observed associated especially with kelp forests and epibenthic predatory or herbivorous fish are also found, e.g. blennies, gobies and wolf fish (Anarhichas lupus).
- Kelp blades support microalgal epiphytes or endophytes such as Pogotrichum filiforme, Chilionema sp. and Myrionema corunnae which is only found on Laminaria blades, as well as Helcion pellucidum and opportunistic hydroids (e.g. Obelia geniculata) and bryozoans (e.g. Membranipora membranacea).
- The stipes may support a diverse fauna and flora, especially foliose red algae, depending on age of the stipe, kelp density (stipes in close proximity may abrade each other) and degree of grazing. Epiphytes show greater biomass on the top 10-20 cm of stipe and exhibit a zonation pattern down the stipe which changes with depth (Birkett et al., 1998b). Norton et al. (1977) found the greatest biomass at 3m depth near Lough Ine. Whittick (1983) showed that epiphyte biomass was significantly greater in plants over 5yrs old, with Palmaria palmata(dulse) dominating the top of the stipe from 1-2m, being replaced by Ptilota plumosa between 6-10m, while Membranoptera alata and Phycodrys rubens dominate below 12m or are present at lower parts of the stipe.. Hiscock & Mitchell (1980) list 15 species of algae associated with kelp stipes in the UK. The stipes also supports epifaunal bryozoans and hydroids (Norton et al., 1977).
- Holdfasts support a diverse fauna that represents a sample of the surrounding mobile fauna and crevice dwelling organisms, e.g., polychaetes, small crabs, gastropods, bivalves, and amphipods. Jones (1971) lists 53 macrofaunal invertebrates in holdfasts and Moore (1973b) reports 389 species from holdfasts collected in the north east coast of Britain. A useful account of holdfast fauna is given by Hayward (1988).
- The composition of the holdfast fauna has been show to vary with turbidity (natural and anthropogenic in origin), between kelp species (due to holdfast architecture and volume), and with location around the coast of the British Isles (Moore, 1973a&b; Moore, 1978; Edwards, 1980; Sheppard et al., 1980). Moore (1973a&b) identified groups of species that were found in most cases, or restricted to either turbid or clear waters. Moore (1978) noted that species diversity or amphipods decreased with increasing turbidity, partly due to the increased dominance of a few species. Edwards (1980) noted that holdfast fauna in south-west Ireland were numerically dominated by suspension feeders with decreasing numbers of omnivores and carnivores respectively. Edwards (1980) noted that holdfasts were dominated by Pomatoceros triqueter in the most turbid sites, although theses were not as turbid as sites examined by Moore (1973a&b). Sheppard et al. (1980) examined 35 sites around the Britain Isles and demonstrated a correlation between heavy metal pollution, turbidity and location. Along the North Sea coast species number and diversity increased with increased clarity, however where heavy metals were a factor species number and diversity decreased with increasing heavy metal pollution. They were able to distinguish groups of species characteristic of all sites, or clear or turbid sties. Along the west coast both heavy metals and turbidity were important. Where turbidity and heavy metals increased suspension feeders increased in abundance while other trophic groups decreased. However, along the south coast longitude was the most important factor, and they suggested that natural variation in temperature, salinity and water flow were responsible for variation between holdfast communities (Sheppard et al., 1980). Moore (1985) also demonstrated that the amphipod fauna varied with water flow rate (resulting from wave action and currents); for example sites of increased exposure were dominated by Amphithoe rubricata, Lembos websteri and Jassa falcata whereas Gitana sarsi, Dexamine thea and Corophium bonnellii flourish in wave sheltered environments.
- A few meiofaunal species may burrow into kelp tissue, e.g. the nematode Monohystera disjuncta (Birkett et al., 1998b).
- The benthic fauna varies with depth, exposure, location and substratum, however, no species are specific to kelp forest. Norton et al. (1977) demonstrate the zonation of 22 epibenthic species. However, many species, both fixed and mobile, are present and probably under recorded (Birkett et al., 1998b).
No specific information found has been found but the communities in this biotope are likely to be highly productive. The biotope occurs in shallow depths where both high light intensity will result in high primary productivity. Kelps are the major primary producers in UK marine coastal waters producing nearly 75% of the net carbon fixed annually on the shoreline of the coastal euphotic zone (Birkett et al., 1998b). Kelp plants produce 2.7 times their standing biomass per year. Kelp detritus, as broken plant tissue, particles and dissolved organic material supports soft bottom communities outside the kelp bed itself. The kelps reduce ambient levels of nutrients, although this may not be significant in exposed sites, but increase levels of particulate and dissolved organic matter within the bed.
The characterizing species in this biotope all have planktonic spores or larvae and are fairly short-lived (five to ten years). There is therefore high recruitment and high turnover. Recruitment processes of key characteristic or dominant species are described here.
- Laminaria hyperborea produces vast numbers of spores, however they need to settle and form gametophytes within about 1 mm of eachother to ensure fertilization and therefore may suffer from dilution effects over distance. Gametophytes can survive darkness and develop in the low light levels under the canopy.
- Recruitment of epiphytes and epiflora are dependant on dispersal and settlement of algal spores and survival of early post-settlement stages. Norton (1992) suggests that spore dispersal is primarily dependant on currents and eddies. Settlement of algal spores is partly dependant on their motility (if any) and adhesive properties together with preferences for topography (surface roughness), the chemical nature of the substratum and water movement (Norton, 1992; Fletcher & Callow, 1992). For the foliose red alga Delesseria sanguinea (which is probably representative of many of the species in the biotope), Dickinson (1963) suggested a life span of 5-6 years but Kain (1979) estimated that 1 in 20 specimens may attain 9 -16 years of age. The spores of red algae are non-motile (Norton, 1992) and therefore entirely reliant on the hydrographic regime for dispersal. Norton (1992) reviewed dispersal by macroalgae and concluded that dispersal potential is highly variable. Spores of Phycodrys rubens, another species found in the biotope, were suggested to travel up to 5 km before settlement.
- For Lithophyllum incrustans , representing the encrusting Corallinacea in the biotope, it has been calculated that 1 mm x 1mm of reproductive thallus produces 17.5 million bispores per year with average settlement of only 55 sporelings/year (Edyvean & Ford, 1984). Dispersal is likely to be in excess of 5 km and spores will settle and new colonies will arise rapidly on bare substratum although growth rate is slow (2-7 mm per annum - see Irvine & Chamberlain, 1994).
- For Echinus esculentus, planktonic development is complex and takes between 45 -60 days in captivity (MacBride, 1914) enabling dispersion over a large area. Recruitment may be sporadic or variable depending on locality; e.g. Millport populations showed annual recruitment whereas few recruits were found in Plymouth populations during studies 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. Bearing in mind that MLR.LhypGz is a northern biotope, the apparent higher recruitment success of Echinus esculentus in the north may be important in creating this biotope.
- Some of the animal species that characterize the biotope may recruit readily and from considerable distances away. For instance, in Alcyonium digitatum, actively swimming lecithotrophic planulae are likely to have an extended pelagic life of several days or weeks (see MarLIN review for full details) before they eventually settle and metamorphose to polyps (Matthews, 1917; Hartnoll, 1975).
- The embryos of Antedon bifida hatch as free-swimming larvae which, after a short pelagic phase, attach to the substratum and develop a short stalk (Chadwick, 1907, cited in Nichols, 1991).
Kelp beds also provide nurseries for larvae and fish species (see above).
Time for community to reach maturity
MIR.LhypGz is a dynamic biotope in which the maintenance of bare Corallinacea covered rock is dependant on grazing. Experimental studies as well as observations of the impacts of urchin grazing in natural communities provide significant information. Experimental clearance experiments in the Isle of Man (Kain, 1975; Kain, 1979) showed that Laminaria hyperborea
out-competed other opportunistic species (e.g. Alaria esculenta
, Saccorhiza polyschides
spp.) and returned to near control levels of biomass within 3 years at 0.8 m but that recovery was slower at 4.4m (see above). Studies of the effects of harvesting in Norway (Svendsen, 1972, cited in Birkett et al.
, 1998b) showed that kelp biomass returned 3-4 years after harvesting, although the plants were small (about 1m) and the age class was shifted towards younger plants. Sivertsen (1991, cited in Birkett et al.
, 1998b), showed that kelp populations stabilise about 4-5 years after harvesting. Current advice suggests that kelp forest should be left 7-10 years for kelp and non-kelp species to recover (Birkett et al.
, 1998b). Detailed studies in Norway by Rinde et al.
(1992, cited in Birkett et al.
, 1998b) examined recovery of non-kelp species. The epiphyte community in control areas about 10 years old was richer and more extensive than on replacement plants in harvested areas. Of the epifauna, Halichondria
sp. were only found on 10 year old plants and tunicates on plants 6 years post harvesting. Holdfast fauna was more abundant richer in 10 year old plants in control areas than younger plants in previously harvested area. Overall his results suggest that full biological recovery, or maturation, may take at least 10 years.
MIR.LhypGz is a dynamic biotope in which the maintenance of bare Corallinacea covered rock is dependant on grazing. In the absence of significant grazing, the biotope would switch to another such as EIR.LhypR.
This review can be cited as follows:
Grazed Laminaria hyperborea with coralline crusts on infralittoral 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=333&code=1997>