Adula simpsoni (Marshall), a bivalve associated with Whale skulls in the North Sea.

The crew of a Scarborough trawler struggle to remove the rotting carcase of a 40ft whale brought up in the trawl; remains of whales and dolphins are frequently seen by trawler crews. Photo donated by Malcolm Ward.

The crew of a Scarborough trawler struggle to remove the rotting carcase of a 40ft whale brought up in the trawl; remains of whales and dolphins are frequently seen by trawler crews. Photo donated by Malcolm Ward.

The rotting or skeletonised remains of whales and dolphins are frequently brought up in the nets of trawlers working round the British Isles. However, it is only in recent years that biologists have discovered that the remains of dead whales, known as whale falls, attract a series of activities of other marine species, that not only reduce the carcase to its bony framework, but which then begin to colonise, and in some recently discovered polychaete worms, also extract nutrients from, its bones.

In the eastern North Atlantic and around the north of Scotland into the North Sea, however, a small bivalve of the mussel family Mytilidae, has long been known to be associated with the remains of whales.

Adula simpsoni has the exceptional habitat of settling in the sutures and inside the craniums of old skulls of whales, where it attaches firmly by means of the byssus threads.The bright yellow-brown shells of Adula are thin, with a glossy, varnished-like periostracum. It grows to a maximum length of 30mm, but shells approaching this size are always corroded, a factor that, given the extremely thin nature of the shells, probably brings about the death of the animal through exposure to predatory invertebrates. Growth stages on the shells are not very obvious, but it is likely that the life-span of Adula is not very long despite the otherwise protective nature of its environment.

The glossy shells of Adula grow up to 30mm long; the mollusc is found on old whale skulls.

The glossy shells of Adula grow up to 30mm long; the mollusc is found on old whale skulls.

Xylophaga, supreme wood-boring molluscs from the Yorkshire coast.

A dense colony of Xylophaga dorsalis, where many of the intervening walls between the burrows have been bored away.

A dense colony of Xylophaga dorsalis, where many of the intervening walls between the burrows have been bored away.

Natural timber carried into the sea from rivers in winter flood, or processed timber in the form of mans ships, boats and lost cargo, form a very special habitat for certain groups of wood-boring bivalve molluscs, of which the most well-known are the ship-worms of the family Teredinidae. A closely related group of molluscs are the wood piddocks, members of the Xylophagidae, whose wood-boring capabilities are just as devastating as those of the shipworms.

Like the shipworms, the shells of the mollusc have lost their function of protecting the soft body, and have become instead, specialised cutting tools with which the post-larval animal rapidly penetrates the timber, and which continue to grow through the life of the animal. The front margin of the shells are cut away to enable the round disc-like foot to grip the head of the boring, while the projecting, curved shell lobes above the foot bear rows of minute cutting teeth that cut a concave path deeper into the timber. Immediately behind these lobes, the sides of the rounded shell also bears lines of teeth, by which the walls of the excavation are simultaneously cut away, leaving, as the animal grows and advances, a perfectly smooth-walled boring through the timber.

Two species of Xylophaga occur in Yorkshire waters, X. dorsalis, and X. praestans.

XYLOPHAGA DORSALIS

The large wood-piddock Xylophaga praestans, contracted in its burrow.

The large wood-piddock Xylophaga praestans, contracted in its burrow.

The most prolific of all the wood boring molluscs is the pea-sized Xylophaga dorsalis, whose erratic borings, running in all directions and cutting across each other, completely demolish the timber, filling their surroundings with a paste of wood particles; it is found at all depths, from the deepest off-shore pits to just a couple of fathoms of water off the coast, and infests even the thin bottoms of traditional crab pots.

XYLOPHAGA PRAESTANS

A much larger species, Xylophaga praestans, is a very special member of our coastal waters in a number of ways. First discovered and described as recently as 1912, it is rarely seen by most biologists and occurs only in the North Sea, and is usually quoted as being a rare species occurring only off the coasts of Northumberland and Durham, but in fact its distribution extends over a much greater area, both north and south. The first, and largest specimen that I examined came from just twelve miles off Scarborough in 1967, but I have, over the years, also seen its borings from many locations, including timber trawled up in the Norwegian sector of the North Sea.

This species can grow to a large size, cutting enormous, beautifully smooth borings up to 30 mm in diameter and over 300mm long, although usually it is much smaller. This first Yorkshire specimen was a solitary individual living in a blackened, sulphide rich piece of tree trunk that was so soft it could be shredded between the fingers, and on its body were bonded the traces of an egg capsule of some other organism that had at one time also occupied the boring, but which defied identification.

Anterior aspect of Xylophaga praestans in its boring, showing the round foot and the projecting anterior lobes of the shell that cut away the timber at the head of the burrow.

Anterior aspect of Xylophaga praestans in its boring, showing the round foot and the projecting anterior lobes of the shell that cut away the timber at the head of the burrow.

The mystery was solved several years later when a large colony of X. praestans was found in a log hauled up from the deep water around Bruceys Garden, near the edge of the Dogger, and where this wood-borer is common. Scattered through the borings and over the wood piddocks themselves were bonded hundreds of tiny brown domes, the egg capsules of a species of flatworm that was finally found by flushing the borings through with preservative. This is a remarkable and previously unknown example of commensalism; the flatworms Taenioplana teredini and Stylochoplana affinis are recorded from empty burrows of Teredo elsewhere in the world, but this appears to be the only such association known in British waters, or with Xylophaga.

Other organisms inhabit the Xylophaga borings including a specialised polychaete that ingests the finely ground wood particles that partially fill the borings.

Xylophaga species, unlike the shipworms, do not digest the wood that they file away, but like related bivalves, filter minute planktonic organisms and detritus out of the surrounding water.

Although sometimes found in dense aggregations, they may also be found in low numbers or even as solitary isolated individuals, and frequently as isolated units at great depth, and the wood piddocks have therefore evolved a different reproductive strategy to other bivalve molluscs. Like the shipworms, smaller younger individuals are male, which as they grow, change to female. Unlike the shipworms however, sperm produced by the males is stored in a special receptacle, and when the animal eventually changes sex, this sperm is used to fertilise the eggs.

Shells of the wood-piddock, Xylophaga praestans.

Shells of the wood-piddock, Xylophaga praestans.

Nudibranch molluscs ( Sea-slugs ) of the Yorkshire Coast & Central North Sea

D. E. WHITTAKER

The nudibranchs belong to that great group of animals known as the Mollusca, which includes the snails, slugs, clams, chitons, limpets, octopus and squid. The bodies of the nudibranchs are without a shell, and the gills, variously carried as veils, branched excresences or plumes on the different species, are therefore totally unprotected, hence the name of the group, the Nudibranchiata, or ‘naked gilled’ molluscs.  Popularly known as sea-slugs, many of these delicate creatures are among the most beautiful and colourful sea-creatures of the British Isles, while tropical species are even more spectacular.

Most British species are small and require careful and laborious searching under boulders on the sea-shore, or among the mass of hydroids and weed brought up in trawl nets. The number of species confirmed as occurring on the Yorkshire Coast is comprehensive, although several other species that are undoubtedly  present in the area have so far evaded observation, due to the difficulties of sampling these molluscs. There have been few workers of this group on this coast, and historical records are few and principally the work of Dr. Irving, who worked the rock pools at Scarborough during the first decades of the twentieth century, while Dr Chris Todd worked the group while a student at the now defunct  Wellcome Marine Laboratory of Leeds University at Robin Hood’s Bay in the mid 1970’s. The present author’s records began during shore work in the early 1960s, extending to offshore material later in the decade.

Reference material in the Archive consists of preserved specimens and photographic records, but close-up video is  now being used to record the animals in situ when found.

Aegires Punctilucens

Aegires Punctilucens - Specimen from the South Bay, Scarborough, Yorks.

Confirmed Yorkshire & Central North Sea species

Dendronotacea

Tritonia hombergi Cuvier, 1803

Tritionia lineata Alder & Hancock 1848

Tritonia plebeia Johnston, 1828

Lomanotus genei Verany, 1846

Lomanotus marmoratus (Alder & Hancock, 1845)

Scyllaea pelagica L., 1758

Dendronotus frondosus (Ascanius, 1774)

Doto coronata (Gmelin, 1791)

A rare North Sea species, this specimen was taken on the shore at Burniston Bay, near Scarborough, Yorks.

Aeolidiella alderi - A rare North Sea species, this specimen was taken on the shore at Burniston Bay, near Scarborough, Yorks.

Doto cuspidata Alder & Hancock, 1862

Doto dunnei Lemche, 1976

Doto fragilis (Forbes, 1838)

Doto hydrallmaniae

Doto koenneckeri Lemche, 1976

Doto pinnatifida (Montagu, 1804)

Doto tuberculata Lemche 1976

Embletonia pulchra Alder & Hancock, 1851

Doridacea

Goniodoris castanea Alder & Hancock, 1845

Goniodoris nodosa (Montagu , 1808)

Armina loveni - Formerly regarded as a rare species around the British coast, this species is common off the Yorkshire Coast; this was the first example found here in 1976.

Armina loveni - Formerly regarded as a rare species around the British coast, this species is common off the Yorkshire Coast; this was the first example found here in 1976.

Okenia aspersa (Alder & Hancock, 1845)

Okenia leachi (Alder & Hancock, 1854

Okenia elegans (Leucart, 1828)

Ancula gibbosa (Risso, 1818)

Acanthodoris pilosa (Muller, 1879)

Adalaria proxima (Alder & Hancock, 1854)

Onchidoris bilamellata (L.,1767)

Onchidoris depressa (Alder & Hancock, 1842)

Onchidoris inconspicua (Alder & Hancock, 1851)

Onchidoris muricata (Muller, 1776)

Onchidoris indet. (a small, purple-spotted species taken on the shore near Scarbough

Onchidoris oblonga (Alder & Hancock, 1845)

Onchidoris pusilla (Alder & Hancock, 1845)

Polycera quadrilineata - Common species on the Yorks. coast, sometimes occurring in large numbers on the shore.

Polycera quadrilineata - Common species on the Yorks. coast, sometimes occurring in large numbers on the shore.

Onchidoris sparsa (Alder & Hancock, 1846)

Aegires punctilucens (Orbigny, 1837)

Limacia clavigera (Muller, 1776)

Polycera quadrilineata (Muller, 1776)

Palio dubia (M. Sars, 1829)

Palio nothus (Johnston, 1838)

Eudoridoidea

Cadlina laevis (L., 1776)

Rostanga rubra (Risso, 1818)

Archidoris pseudoargus (Rapp, 1827)

Discodoris planata ( Alder & Hancock, 1846 )

Jorrunna tomentosa (Cuvier, 1804)

Arminacea

Armina loveni (Bergh, 1860)

Janolus cristatus (Chiaje, 1841)

Janolous hyalinus (Alder & Hancock, 1854)

Hero formosa (Loven, 1841)

Aeolidacea

Coryphella browni Picton, 1980

Coryphella gracilis (Alder & Hancock, 1844)

Coryphella lineata (Loven, 1846)

Corryphella verrucosa (M. Sars, 1829)

Aeolidiella glauca, a common off-shore nudibranch.

Aeolidiella glauca, a common off-shore nudibranch along the Yorkshire coast; video still image.

Flabellina pedata (Montagu, 1815)

Cuthona amoena (Alder & Hancock, 1845)

Cuthona caerulea (Montagu, 1804)

Cuthona foliata (Forbes & Goodsir, 1839)

Cuthona genovae (O’Donohue, 1926)

Cuthona nana (Alder & Hancock,1842)

Cuthona pustulata (Alder & Hancock, 1854)

Cuthona rubescens Picton & Brown, 1978)

Cuthona viridis (Forbes, 1840)

Catriona gymnota (Couthony, 1838)

Tennellia adspersa (Nordmann, 1845)

Tergipes tergipes (Forskal,1775)

Calma glaucoides (Alder & Hancock,1855)

Onchidoris inconspicua, a rarely seen species from between tide-marks, Burniston bay near scarborough.

Onchidoris inconspicua, a rarely seen species from between tide-marks, Burniston bay near scarborough.

Eubranchus exiguus (Alder & Hancock, 1848)

Eubranchus pallidus (Alder & Hancock, 1842)

Eubranchus tricolor Forbes, 1838

Facelina bostoniensis (Couthony, 1838)

Facelina coronata (Forbes & Goodsir,1839)

Aeolidia papillosa (L., 1761)

Aeolidiella alderi (Cocks, 1852)

Aeolidiella glauca (Alder & Hancock, 1845)

Nudibranchs as the prey of Fishes on the Yorkshire Coast

Lacking a shell, the soft bodied nudibranchs utilse a number of defensive mechanisms to avoid predation, including the storage and deployment of stinging cells, derived from the tissues of the anemones and hydroids they devour, the use

Some of the nudibranchs found in the stomach of a gorged black bream, Spondyliosoma. Those shown here include Dendronotus and Lomanotus.

Some of the nudibranchs found in the stomach of a gorged black bream, Spondyliosoma. Those shown here include Dendronotus and Lomanotus.

of calcareous spicules embedded in the surface tissues, and the production of acidic and mucous secretions from special glands, while many species are also thought to exhibit warning colouration. Many others are cryptically coloured, marked, or sculpted and become very difficult to determine in their particular habitat; Aegires punctiluscens, for example, is extremely difficult to detect and its presence is often only revealed by the egg masses they have deposited nearby.

Nudibranchs are sometimes attacked and eaten by the pycnogonids, or sea-spiders, that frequent the hydroids upon which many nudibranchs also prey. However, it is invariably stated that nudibranchs are not eaten by fishes, because of their supposed unpalatability due to the various defence mechanisms listed above. Experiments on the feeding of nudibranchs to fishes at the Plymouth laboratory early in the 20th century are frequently cited as evidence to this view, further supported by the absence of reports of their discovery in the stomachs of fishes.

A sample of many hundreds of Facellinid nudibranch remains from haddoch stomachs off the Yorkshire coast.

A sample of many hundreds of Facellinid nudibranch remains from haddoch stomachs off the Yorkshire coast.

Observations on the Yorkshire coast, however, show that certain fishes regularly devour nudibranchs, sometimes in large numbers.

The black sea bream, Spondyliosoma cantharus, the most commonly found spariid in the North sea, is an occasional trawl catch on the Yorkshire coast. Stomach contents of Yorkshire examples of this fish were examined by simple visual inspection until 1974, when an almost intact specimen of the nudibranch Eubranchus tricolor was found as a prey item in a young fish. It was realised that had the mollusc been in a more advanced state of digestion, or considerably smaller, it would not have been recognised as a nudibranch or perhaps, even as a mollusc, by the naked eye. Had the mollusc been completely digested, the tiny radula and jaws would have gone entirely unnoticed, and thus the presence of nudibranchs as prey items in previous  Yorkshire catches of Spondyliosoma had been overlooked. Dating from this occurrence, all Spondyliosoma  samples have therefore been critically examined under the microscope. It was also apparent that this prey item would not have been recognised by anyone unfamiliar with living or preserved members of the group.

Facellinid nudibranchs from Haddock stomach off Scarborough; cerata are still present on many of the molluscs.

Facellinid nudibranchs from Haddock stomach off Scarborough; cerata are still present on many of the molluscs.

These factors therefore underlie the difficulties of recognising and identifying the remains of nudibranchs in fish stomachs,and which has assisted the prevailing view that as a group they are unpredated by fishes. It should be further realised that the majority of fisheries biologists conducting stomach analyses have no familiarity of the nudibranchiata, the majority of which are of small size, nor is it regular practice to laboriously examine the finer detritus of  the stomachs of demersal fish, unless conducting parasitological studies, and which is essential for the detection of nudibranch radulae and jaws.

Further examinations of  Spondyliosoma caught in this sea area have revealed a number of species of nudibranch are eaten, including one fish being gorged upon several species, belonging to several families, to the exclusion of other types of prey.

Large specimens of Aeolidia, recently devoured, have been found in the cod, while the even larger Tritonia hombergi, a common mollusc on the local trawling grounds, is frequently eaten by both cod and haddock along the Yorkshire coast, the large, unmistakable jaws being easily seen by the naked eye; this sea-slug has of course long been known to be devoured by Scyliorhinus caniculus, the lesser spotted dogfish, elsewhere in the British Isles, though the stomach contents of the Yorkshire population of this fish  have not been investigated.

The haddock devours a wide range of benthic animals on the Yorkshire grounds, including many molluscs, and in particular large numbers of the opisthobranchs Pleurobranchus, Cylichna ,Retusa and Philine, but in the summer of 2005 was also discovered to be predating large numbers of nudibranchs, easily recognised from the many partially digested remains as being facellinids, at a particular off-shore locality. A small sample of gut detritus from  this catch of haddock, examined microscopcally, further revealed many hundreds of facellinid jaws and radulae, indicating not just the large scale cropping of the molluscs by the haddock, but also the huge numbers of these nudibranchs present on the sea bed at this particular locality at that season.