Where several species of burrowing megafauna occur together in the same habitat it is not uncommon for burrows to interconnect, and some quite complex multi-species systems have been revealed by resin-casting. Examples include burrow complexes of Cepola rubescens with Goneplax rhomboides and Callianassa subterranea (Atkinson et al., 1977), Nephrops norvegicus with Goneplax rhomboides and Lesueurigobius friesii (Atkinson, 1974b), and Nephrops norvegicus with Maera loveni (Atkinson et al., 1982). Interspecific connections are very common in some localities. Tuck et al. (1994) found that 34% of Nephrops burrows at a site in Loch Sween showed evidence of interactions with other species, including Maxmuelleria lankesteri, Jaxea nocturna and Lesueurigobius friesii, while 22% of the Maxmuelleria burrows examined by Nickell et al. (1995a) were connected with those of Jaxea nocturna. In some of the latter cases the Maxmuelleria and Jaxea shared the same burrow opening.

These interconnections are likely to be accidental in most cases and not indicative of any close symbiotic relationship between the different burrowers. However, once made, it is likely that connections will be maintained for their nutritional and ventilatory advantages. For example, a species such as Jaxea nocturna may benefit from association with Maxmuelleria lankesteri by taking advantage of the organic-rich surface sediment pulled into the burrow by the worm.

The interactions within megafaunal burrowing communities are still too poorly-known to say whether the presence of particular species has any positive or negative effects on the abundance of others. Nephrops norvegicus has been observed to prey on Calocaris macandreae (Smith, 1988), and will probably eat any of the other thalassinidean species if encountered. However, high densities of Nephrops and Calocaris coexist in many localities (Chapman, 1979). It is possible that the digging activities of Nephrops norvegicus may very occasionally unearth specimens of Maxmuelleria lankesteri (personal observations), leading to the demise of the worm, which is probably unable to re-burrow when exposed.

It is conceivable that sea pens might be adversely affected by high levels of megafaunal bioturbation, perhaps by an inhibitory effect on the survival of small, newly-settled colonies. Sea pens and various species of burrowing megafauna certainly coexist in many localities, but so far there has been no investigation of the interaction between them.

A variety of small benthic animals will take advantage of the shelter offered by megafaunal burrows, especially when these are long-lasting or permanent structures. Echiuran burrows in particular have been found to harbour a rich associated fauna (Fisher & MacGinitie, 1928; Ditadi, 1982). Nickell et al. (1995a) found that numerous small bivalves and polychaete worms colonized the walls of Maxmuelleria lankesteri burrows. Mobile polychaetes such as Ophiodromus flexuosus, which normally live out on the sediment surface were also seen to enter burrows. A similar commensal fauna has been recorded in burrows of Echiurus echiurus in the German Bight (North Sea) (Rachor & Bartel, 1981). In most cases the commensal organisms also occur as part of the ‘background’ sediment fauna and are not obligate burrow residents. Within burrows they probably benefit from the echiurans’ irrigation activities which supply both oxygenated water and food, and may additionally gain some refuge from predators.

Thalassinidean burrow walls are probably a less suitable habitat for commensals because of the continual reworking and sediment grazing activities of the crustacean occupant. However, the body of the mud-shrimp itself may offer a substratum for colonization. The ctenostome bryozoan Triticella flava grows as a dense ‘furry’ covering on the antennae, mouthparts and legs of burrowing crustaceans. It occurs most commonly on Calocaris macandreae, but has also been found on Nephrops norvegicus, Goneplax rhomboides, Jaxea nocturna and Upogebia spp. On Calocaris macandreae, the bryozoan coverage is densest in late summer, but is shed when the crustacean moults its exoskeleton in September-October (Buchanan, 1963). However, the reproductive cycle of Triticella is synchronized with the moult cycle of its host and larvae are available to recolonize the crustacean body after the moult (Eggleston, 1971).

A truly remarkable commensal organism was described in 1995 from the mouthparts of Nephrops collected in the Kattegat, Denmark (Conway Morris, 1995). This organism, named Symbion pandora, is a tiny sessile animal less than 1 mm long with a basal attachment disc and an anterior ciliated food-gathering organ. It has a complex life-cycle involving both sexual and asexual stages. In the details of its structure, Symbion is so different from anything described previously that its discoverers created an entirely new phylum (Cycliophora) to contain it (Funch & Kristensen, 1995). Since the animal kingdom includes only about 35 phyla (each representing a major basic body plan), the description of a new one is a significant zoological event. Its association with Nephrops norvegicus illustrates that even relatively well-known organisms can still yield surprising discoveries.

A few organisms have also been recorded in association with the British sea pens. The isopod crustacean Astacilla longicornis has a specialised, highly elongate body form and is sometimes found clinging to the rachis of Funiculina quadrangularis. Another associate of Funiculina is the brittlestar Asteronyx loveni, a species which uses its very long, prehensile arms to cling to the sea pen, so maintaining itself in an elevated position above the sea bed (Fujita & Ohta, 1988). Asteronyx is a deep-water form usually found below 100 m depth. In British waters it has been sporadically recorded from the west of Scotland, but Loch Hourn holds the only precisely-located inshore population (Dr J.D. McKenzie, personal communication).

In addition to the megafaunal burrowers and sea pens, the biotopes within this complex support a variety of large animals living on or just below the sediment surface. The burrowing anemone Cerianthus lloydii is common throughout British and Irish waters in a wide range of sediment types. The much larger Pachycerianthus multiplicatus has a very localised distribution on the western Scottish and Irish coasts (it is also known from Scandinavia). This species is characteristic of the deep mud biotopes CMU.SpMeg and CMU.SpMeg.Fun. Howson et al. (1994) listed it as present in only 16 of the 98 sea lochs covered in their report. The densest known populations are at the heads of Lochs Fyne (Howson & Davies, 1991) and Duich (Connor, 1989). These two anemones inhabit tubes embedded in the sediment and so are not strictly ‘epifauna’. Another large (non-burrowing) anemone sometimes recorded on Nephrops grounds is Bolocera tuediae. This anemone has frequently been seen surrounded by aggregations of pink shrimps, Pandalus borealis, (C.J. Chapman, personal communication), but the details of this association are not known.

Common epibenthic predators/scavengers occurring in these biotopes include shore crabs Carcinus maenas, edible crabs Cancer pagurus, swimming crabs Liocarcinus depurator, hermit crabs Pagurus bernhardus and the starfish Asterias rubens and Crossaster papposus. The surface-living brittlestars Ophiura ophiura, O. albida and O. affinis are common on the sandier mud biotopes (CMS.VirOph, CMS.VirOph.HAs) and present in lower numbers on the finer muds. The white, slug-like gastropod Philine aperta is often present at very high densities (> 100 m^-2) on the finer substrata. This species is a predator of polychaete worms, bivalves and foraminiferans at the sediment surface.

Most of the common inshore fish species can be encountered over soft mud biotopes but seldom in large numbers. The biotope complex is not a major habitat for any commercially-important species. Aside from the specialist burrowers, the most characteristic fish are probably the gobies Gobius niger and Potamoschistus minutus.

Little is known about the intensity or importance of predation on the characteristic species of the biotope complex. Birkeland (1974) described a complex interaction between the sea pen Ptilosarcus guerneyi and seven predator species (four starfish and three nudibranchs). In British waters the nudibranch Armina loveni is a specialist predator on the sea pen Virgularia mirabilis. This sea slug is infrequently recorded, but is known to occur from Norway to western France. In Puget Sound, a related species, Armina californica is one of the predators of Ptilosarcus guerneyi. Birkeland (1974) found that the nudibranch fed preferentially on the largest sea pens. In the laboratory, individuals were found to eat an average of one Ptilosarcus every four days. Armina was an uncommon animal at the study site and its impact on the sea pen population appeared to be minimal. Another predator on Ptilosarcus was the sun star Crossaster papposus. This species is also common in British waters and so may be a potential predator on sea pens here. Amphipod crustaceans of the family Stegocephalidae also appear to feed on sea pens, but little is known of their ecology (Moore & Rainbow, 1984).

Many specimens of Virgularia mirabilis lack the uppermost part of the colony, a feature which has been attributed to nibbling by fish. Mackie (1987) found that extracts of Pennatula phosphorea inhibited feeding in sole Solea solea, suggesting that this sea pen may possibly have a chemical defense against fish predation.

Nephrops norvegicus is known to be eaten by a variety of bottom-feeding fish, including cod, haddock, skate and dogfish. In some areas up to 80% of cod stomachs are found to contain Nephrops (Howard, 1989). There are also numerous records of fish predation on thalassinidean mud-shrimps, for example Buchanan (1963), who found Calocaris macandreae in the stomachs of cod Gadus morhua and haddock Melanogrammus aeglefinus. Since these mud-shrimps rarely if ever appear on the sediment surface, the fish probably catch them by suction while they are engaged in activities (eg. sediment expulsion) in the upper reaches of their burrows. The echiuran Maxmuelleria lankesteri has also been recorded in the stomachs of Irish Sea cod. Rachor & Bartel (1981) found that Echiurus echiurus was an important food for fish in the German Bight.

The burrowing megafauna and larger epifauna of these biotopes are accompanied by a a diverse fauna of smaller animals living within the sediments. Animals retained by a sieve of 0.5 mm mesh size are classed as ‘macrofauna’ (those passing through a sieve of this grade fall within the ‘meiofauna’ and ‘microbiota’). The macrofauna of marine sediments has generated an enormous literature, particularly in the field of benthic pollution monitoring (review in Pearson & Rosenberg, 1978), and only a brief outline of its composition relevant to the general ecology of the biotope complex can be given here.

The organic-rich fine muds supporting the biotopes within this complex (CMU.SpMeg and CMU.SpMeg.Fun) will typically support 30 - 45 macrofaunal species in areas not suffering from gross organic pollution. The macrofauna is found largely in the top 10 cm of sediment, with a majority of individuals in the uppermost 3 cm. Polychaete worms usually dominate in number of species and individuals. Members of the families Spionidae (eg. Prionospio spp.) and Cirratulidae (eg. Chaetozone setosa, Tharyx spp.) are often the most common taxa. In samples from Loch Sween, spionids and cirratulids comprised up to 70% of the individual animals present (personal observations). These are all small slender worms, 2 - 3 cm long, which use long anterior palps or tentacles to collect organic particles in the sediment. Other small polychaetes important in this environment are Scalibregma inflatum, and species of the genera Glycera, Nephtys and Pholoë. Small bivalves such as Mysella bidentata, Corbula gibba and Abra alba may be abundant. Other groups frequently present in large numbers are nemertean and phoronid worms. The brittlestars Amphiura filiformis and A. chiajei are also often common, with A. chiajei predominating on the finer muds. Most of these animals are deposit-feeders, ingesting tiny organic particles and feeding on the bacterial layer coating the sediment grains. Suspension-feeders include Amphiura filiformis and Corbula gibba.

Other biotopes within the complex will also support a polychaete and bivalve-dominated macrofaunal community, but the mix of species will differ according to hydrodynamic conditions, sediment type and level of organic enrichment. In general, more suspension-feeding animals will be found as the sediment grade becomes coarser. The sandier muds with Virgularia mirabilis (biotope CMS.VirOph) will also usually have the Amphiura species in large numbers (with A. filiformis predominating), along with the large tube-dwelling polychaetes Chaetopterus variopedatus and Lanice conchilega. Other important polychaetes include Goniada maculata, Nephtys incisa and Notomastus latericeus. The three bivalve species mentioned in the fine-mud fauna above are also frequently common in this biotope.

Most of the typical macrofauna of British sediments have very wide or even cosmopolitan distributions. The unusual polychaete Sternaspis scutata is limited to the southern English examples of biotope IMU.PhiVir, but has a very broad distribution outside the British Isles.

A phenomenon often reported in surveys of sediment macrofauna is the high level of spatial patchiness in species distribution and abundance. Cores taken less than a metre apart may show striking differences in faunal composition. Small-scale differences in sediment characteristics undoubtedly contribute to this variability, for example where localized patches of highly-enriched sediment are created by the decomposition of loose seaweed or other organic detritus. However, the sediment fauna itself may help to generate this spatial variability, a key factor being the disturbance to the sea bed (bioturbation) caused by the activities of the large burrowing megafauna. Where they occur in large numbers, megafaunal burrowers can have a profound influence on their environment. In the southern North Sea, Callianassa subterranea was estimated to turn over a total of 11 kg dry sediment m^-2 year^-1 (Rowden & Jones, 1997), while in an Adriatic lagoon, the volume of water pumped through burrows by Upogebia pusilla during periods of neap tides almost equalled the inflow of water from the open sea (Dworschak, 1981).

Many studies have examined the effects of bioturbation on the smaller sediment fauna (Hall, 1994). Both enhancing and inhibitory effects have been found, depending on the identity of the larger burrowers and the nature of their activity. By constructing and ventilating burrows, megafauna may oxygenate the sediments and make them less compact by virtue of their bodily movements and digging activities. This will allow macrofauna to occupy otherwise uninhabitable deeper sediments and may locally enhance the food supply by stimulating bacterial growth. Thomsen & Altenbach (1993) found that the numbers and biomass of bacteria and foraminifera were up to three times higher around burrows of Echiurus echiurus than in the surrounding sediment. Enhancement of macrofaunal diversity and abundance has been recorded in sediments colonised by dense populations of enteropneust worms (Flint & Kalke, 1986) and echiurans (Rachor & Bartel, 1981; Stull et al., 1986), with a marked decline in community diversity following the disappearance of these larger burrowers.

Negative effects of burrowing megafauna on macrofaunal populations may arise directly by predation, or indirectly as a result of burial, increased turbidity or sediment compaction. Posey (1986) found that most sedentary macrofauna were much less abundant in a dense Callianassa bed than in adjacent areas with fewer Callianassa. Core samples taken from the vicinity of Nephrops norvegicus burrows and from nearby unburrowed sediment showed that the abundance of macrofauna was reduced in near-burrow areas (Smith, 1988) Tentaculate surface-feeding polychaetes were particularly affected. Laboratory observations suggested that these were excluded by the sediment ‘bulldozing’ activities of the crustaceans. However, a number of small, opportunistic nematode and oligochaete worm species were able to take advantage of this and colonize the disturbed patches.

The overall conclusion to be drawn from these studies is that a mix of megafaunal burrowers occurring in a sedimentary biotope will generate a complex and continually-shifting ‘mosaic’ of habitat patches experiencing different types and levels of disturbance. The differing responses to macrofaunal species to this patchiness will probably be a factor in the maintenance of local species diversity. The depth penetration and total abundance of fauna in the sediment may also be enhanced by the physical and chemical consequences of megafaunal activity. However, studies undertaken to date have provided no evidence that any single megafaunal burrower acts as a ‘keystone’ species whose activity is the dominant factor in determining the structure of the local biological community.

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