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DECAY AND FOSSILIZATION OF NON- MINERALIZED TISSUE IN COLEOID CEPHALOPODS by AMANDA J. KEAR, DEREK F. G. BRIGGS and DESMOND T. DONOVAN ‘Anstaact. Decay experiments were caried out on three Recent species of eoleoid cephalopods (the squids AllotenthissubulatasndLoligo forbes, and the sepioidSepiolsalamic) over a petiod of 1 day to 50 weck ‘The morphological sequence of degradation and the fate ofthe more decay resistant organs (beaks, suckers, gidis, statliths, eye lenses) were recorded. Crystalline magnesium phosphate precipitated, but uss tlrastracture was not preserved, Sex aid stage of maturity may ialluence rate of degradation. Differences in buoyancy mechanism, physiological changes during reproduction, and postmortem decay processes alfest the highly variable preservation potential of madera coloids ‘Of the six gencra Belemnotheuts, Mastgophora, Loligsepia,Geopets, Pesoteuths and Trachytewhis) of exceptionally preserved Jurassic fossil coleoids examined for evidence of ultrastructural preservation, ‘Mastigophora exhibits a continuous series of Ussues fom the outer tune, through the mantle and gladius the enuscula sheath ofthe digestive gland. In Belemnorhews and Masigophora the radial and ireular muscle, the outer collagecous tunie and the supporting meshwork of intramuscular fibres are all preserved, Longitudinal fibres are evident in the arms and inthe mantle of some specimens. The texture ofthe calcium ‘Phosphate replacing the soft-tisue varies even within a specimen. Muscles may be represented by the fibres, fron te sreolemma, The microspheres of calcium phosphateare 1-2 ym in diameter inthe former (perhaps represcating the microbes themselves), but only 0-1 4am in the later (where precipitation 3s induced by ‘mlrobial processes). Mirospheresin the tunicare 'S-025 ymin diameter. Muscle unc, intramuscular fibres tnd ink ate preserved in caeium phosphate. Gladius matenal is finely banded, with varying proportions of ‘iagenetccalcim phosphate and calcium carbonate in each ofthe layers in Geopellis rom Charmouth. The mantle morphology found in Mastigophora and Belomnorheutscoreesponds with that found in ving coleoid ‘cephalopods and indicates that this structure had evolved by the Early Jurassic. Ths alls into question the pci oan of Smut «member of te Belem, Ti er fa pan of structural deal fs not confined to small number of unusual locals. There is considerable potential for histologieal investigations of the sftiseues ofa range of extinct organisms. ‘Tar Coleoidea, typified by the extant squids, cuttlefish and octopus, rank alongside the Nautiloidea and Ammonoidea asthe third major subclass of cephalopods. Whilst the nautiloids and ammonoids have a heavy external shell, most coleoids, with the exception of the living families Sepiidae and Spirulidae and the extinet order Belemnitida, have negligible mineralized tissue and are essentially soft-bodied. Nevertheless the soft tissues of coleoid cephalopods are preserved at a aumber of Jurassic localities (Table 1), eg. Holamaden (Toarcian), Germany ; Christian Malford (Callovian), England (Donovan 1983; Allison 1988; Page 1991; Donovan and Crane 1992); Voulte-sur-Rhone (Callovian), France (Fischer and Riot 1982a, 6); Solnhofen (Tithonian), Germany (Bandel and LLeich 1986; Meh! 1990), as well asin the Cretaceous (Albian) of NW Queensland (Wade 1993), the Carboniferous Mazon Creek biota of Ilinois (Allison 1987) and possibly the Devonian (Emsian) Hunsrickschiefer of Germany (Stirmer 1985). Whilst the morphology of a number of coleoids that preserve traces of the soft parts has recently been described in detail from these localities, the ‘mineralization ofthe soft-tissues has only been subjected to preliminary investigation (Allison 1988: ‘Mehl 1990), The aim of this study is to idemtify the tissue types preserved in coleoids, to determine the degree of morphological detail preserved, and to interpret this in the light of controlled decay Pacman oP 11995, 1-130) 1 The Patent Aton 106 PALAEONTOLOGY, VOLUME 38, ‘Tante 1. Types of soft tissues reported in fossil coleoids. —, feature is not preserved; 2, feature may be preserved: n/a, feature would not normally oveur in the coleoids represented in this fauna. Sources of fnformation’ Fischer and Rio 19822: Donovan 1983; Bande and Leich 1986; Alison 1987, 1988; Mehl 1990; Donovan and Tentacles Jaws Gills ‘Tak sae Gladius Locality Solnhofen 2 Present Present Present Present Voolte-sue Present Present — Prescot Preseat Proent = recat Preseat = Present Present = - Present Present aa Present ? Preset ‘experiments on recent cephalopods. Only when the decay process is understood can fossil tissue be reliably interpreted by comparison with living analogues. This has allowed the evolution of mantle tltrastructure in eoleoids to be analyzed, Controls on mineralization were investigated in other ‘experiments using smaller animals (polychaetes and shrimps) which are more easily obtained and processed in the sample sizes required (Briggs and Kear 19934, 1993, 1994; Briggs et al. 1993). COLEOID HISTOLOGY AND ULTRASTRUCTURE Living coleoids have a range of structural tissues of differing composition and resistance to decay (Table 2). The chitin of the buccal mass and digestive system is interconnected and may form a continuous sheet (Kear 1990), starting atthe inner surfaces of the lips and encompassing the beaks, hyaline shield of the radula, buccal palp surface and teeth, and oesophageal and stomach lining. Lip chitin has only been reported in adult Mesonyehoteuthis (Kear 1990) The radular teeth, which erignate spar to he hyaline shield (Nixon 196) and ier in composition, ay not be prt this continuum. ‘Secretion and tanning of the chitin in beaks is carried out by epithelial ess known as beceublasts (Dilly and Nixon 1976), which act as holdfasts for the mandibular muscles (Dilly and Nixon 1976), ‘as well as performing a seretory function. Similar ‘chitinoblas’ cells ae found in association with the radula and hyaline shield (Nixon 1968), buceal palps, oesophagus and possibly the papillary shield (Kear 1990) “The muscular mantle of coleoids is used for both propulsion and respiration. The mantle of the Decapoda (= Decabrachia) (Text-fig. 1) is composed of a thick layer of circular muscle partitioned into bands by thin sheets of radial muscle (Ward and Wainright 1972; Bone ef al. 1981) Longitudinal muscles have only been observed in Sepia officinalis (Bone et a. 1981). Layers of parallel collagen fibres (Text-fig1) encase the mantle muscle, running around the mantle (the inner land outer tunics) in alternate left and right-handed helies (Ward and Wainright 1972). In addition, there isa network of intramuscular connective tissue within the mantle (Ward and Wainright 1972; Bone 1981). This ise consists of fibres composed of collagen (Bone et af. 1981; Gosline and Shadwick 1983) and possibly elastin (Bone er al. 1981) and forms a mesh throughout the muscle (Cext-fig 1). The tunies and mesh resist length changes in the mantle during contraction (Ward and Wainright 1972), Decapod coleoids (Teuthida, Sepiida and Sepiolida) have four pairs of arms and one pair of tentacles; the latter are a specialist prey capture mechanism with suckers present only on the KEAR EY AL: COLEOID CEPHALOPODS 1 ‘Tarte 2, Location and composition of the main structural tissues (where present) in Living coleoid cephalopods, Tssuc/organ Composition Author ‘Suckers and/or hooks Betitin ‘Hunt and Nixon 1981 Lp lining Chin type) Kear 1950 Be chitin Hoont and Nixon 1981 Radula chitin Hunt and Nixon 1981 Hyaline shold chitin Orype)| Bxcal pap teeth ‘chitin Hunt and Nixon 1981 esophagus lining Chaitin (type) Kear 1990 Stomach pein Rudall and Kenchiogton 1973, beehitin Rudall and Keachington 1973; Hunt and Nixon 1981 Brain and nuchal cartilage Collagen Ness 1987 Staliths Aragonite ye Tenses Crystallin Mantle locking cartilage Collagen Ness 1987 Giadivs Bestia Radall and Kenchington 1973; Hunt and Nixon 1981 Internal shell alien ebitin Skin tubercles Collagen Ness 1987 ‘Tunics of mantle muscle Collagen Ward and Wainright 1972; Bone e al. 1981 Gosline and Shadwick 1983 Tnramuscular mesh Collagen Bone ef al. 1981; Gosline and Shadwick 1983, Elastin Bone el. 1981 terminal portion. In resting position the tentacles are retracted within the cone ofthe arms, or into special pouches (eutleish). Certain species of squid only possess tentacles as juveniles. The ‘musculature of both arms and tentacles is more complex than that of the mantle, consisting of longitudinal, transverse, circular, oblique and helical muscle (Kier 1982, 1988), the last in the tentacles only. “The musclar tissues may undergo substantial morphological changes as a coleoid matures. A ‘number of species resorb their own tissues particularly mantle, tentacles and arms to provide ‘energy and resources for gonad growth. This is scen at its most extreme in the squid Moroteuthis ‘ingens, in which immature females have thick (up to 10 mm), muscular mantle walls, but mature individuals have a thin, gelatinous mantle (Jackson and Mladenov 1994). Histological ‘examination reveals that the tissue breakdown is due to a loss of muscle, leaving only the intramuscular collagen fibres intact. In spent (ie. postspawning) individuals even the collagen breaks down. None of these changes is as extreme in males of the same species (Jackson and Miladenov 1994) In contrast, species which need to retain swimming ability for long migrations to pavining grounds show no loss of mantle integrity with maturation (e.g. lex argentina; Clarke et al. 1994), ‘There are phylogenetic contrasts as well. In neutrally buoyant families, such as the Architeuthidae and Histiotcuthidae, active swimming ability is not needed, and only the fins and tentacles are Strongly muscular, Similarly, in some of the oceanic octopods (eg. Cirroteuthidae, Vitrele-