Iain Wilkie - Academia.edu (original) (raw)

Papers by Iain Wilkie

Marine Biodiversity Records, 2010

Certain starfish have a restricted autotomy region at the base of each arm, at which the whole ar... more Certain starfish have a restricted autotomy region at the base of each arm, at which the whole arm is detached if damaged ortrapped. These species are common prey items of gulls, which have been observed to break-up starfish by gripping one arm andshaking the whole animal. This raises the possibility that shaking invokes the autotomy response, thereby acceleratingconsumption of prey

Journal of Zoology, 2009

Although ophiuroid arm shedding has long been accepted as an example of autotomy, there has been ... more Although ophiuroid arm shedding has long been accepted as an example of autotomy, there has been little investigation of the phenomenon to substantiate this. This paper describes the outwardly visible aspects of autotomy and the function of the internal components of the arm during detachment. Observations are focussed on Ophiocomina nigra, some comparisons being made with eight other species.Ophiuroid autotomy is characterized by its occurrence close to the point of stimulation, its rapidity, and by the pattern of intervertebral muscle separation at the insertions which is constant for a given species. Evidence is presented showing the important role played by the intervertebral ligament. Both this and the muscle insertions are collagenous, and it is suggested that they and the other intersegmental connective tissues facilitate autotomy by undergoing a drastic, nervously mediated loss in tensile strength which enables the animal to part from its arm with a minimum of effort. Comparable properties have been ascribed to other echinoderm connective tissues, and their role in asteroid and holothurian autotomy has been acknowledged, but such a mechanism has not previously been suggested for ophiuroid arm autotomy.

Journal of Zoology, 1993

In the present analysis experimental results and computer modelling have been used to compare bio... more In the present analysis experimental results and computer modelling have been used to compare biomechanics of the two most contrasting lantern types among regular echinoids, i.e. the cidarid-type (Stylocidaris affinis) and the camarodont (Paracentrotus lividus) lantern. The lantern is modelled as a rigid pyramid anchored in the centre of the peristomial area. Each side is connected to the test by means of muscles (protractors and retractors) rind ligaments (compass depressors). The overall movement of the lantern may be resolved into vertical displacement and lateral tilting. Computer-aided mechanical analysis of the system takes into account the action of protractor and/or retractor muscles, their elastic reaction and the interaction with the ligamentous structures (peristomial membrane and compass depressors). The geometrical parameters have been determined by preliminary structural analysis and the values of active and passive forces have been measured experimentally. The results of simulations highlight important differences in the mechanics of the Stylocidaris lantern compared to that of Paracentrotus: (1) a very much greater antagonistic effect of muscular passive stretch resistance on lateral tilting: (2) a minor role of the peristomial membrane tensile strength and muscular activity in controlling vertical lantern displacement: (3) a less efficient lantern retraction and protraction owing to unfavourable muscle insertion position on the perignathic girdle and ineffective muscular contraction forces. As a conclusion, in Stylocidaris the action of the protractor and retractor muscles seems to play no significant role in moving the overall lantern, their action being mainly exerted to stabilize it. On the contrary, in Paracentrotus such stabilizing action is provided by the compass depressor ligaments. Finally, on theoretical grounds the arrangement of muscle attachments around the perignathic girdle in Stylocidaris seems to be just as good as that of Paracentrotus for controlling overall lantern mobility, if relative heights of insertions are ignored.

Zoomorphology, 2000

The exterior coelomic septum (ECS) is a mesentery-like structure that encloses the lantern of reg... more The exterior coelomic septum (ECS) is a mesentery-like structure that encloses the lantern of regular sea-urchins and connects it to the inner surface of the test. This paper describes the ultrastructure and microarchitecture of the ECS in Stylocidaris affinis (Cidaridae, Echinoida) and provides information on its contractile and passive mechanical properties. The ECS forms five interambulacral pouches each of which has adthecal (test-facing) and adambulacral (ambulacrum-facing) walls. The ECS wall comprises two coelothelia separated by a layer of connective tissue. The outer coelothelium is a single layer of monociliated cuboidal peritoneocytes and basally located axon-like processes. The inner coelothelium is a single layer of squamous peritoneocytes overlying axon-like processes and, in the adthecal regions only, parallel arrays of elongated myocytes orientated obliquely or horizontally. The intraseptal connective tissue consists mainly of collagen fibrils with sparsely distributed spherule cells and cells containing heterogeneous vesicles. In the adambulacral regions of the ECS hollow beaded microfibrils 20–23 nm in diameter form fibre-like aggregations. This layer also contains calcite spicules of variable size, shape, abundance and orientation. Isolated preparations of the ECS show concentration-dependent contractile responses to K+ ions and acetylcholine. The magnitude of the contractile force varies with the vertical position of the lantern (which determines the starting length of the ECS) in an unusual pattern. Cyclical loading-unloading tests indicate that, as the lantern is raised, the ECS shows low stiffness until the lantern reaches its normal resting position. It is concluded that the adthecal regions of the ECS help to set a limit to lantern retraction and that their contractility assists the protractor muscles in exerting a downward pull on the lantern.

The mutable collagenous tissue (MCT) of echinoderms can undergo extreme changes in passive mechan... more The mutable collagenous tissue (MCT) of echinoderms can undergo extreme changes in passive mechanical properties within a timescale of less than 1 s to a few minutes, involving a mechanism that is under direct neural control and coordinated with the activities of muscles. MCT occurs at a variety of anatomical locations in all echinoderm classes, is involved in every investigated echinoderm autotomy mechanism, and provides a mechanism for the energy-sparing maintenance of posture. It is therefore crucially important for the biology of extant echinoderms. This chapter summarises current knowledge of the physiology and organisation of MCT, with particular attention being given to its molecular organisation and the molecular mechanism of mutability. The biotechnological potential of MCT is discussed. It is argued that MCT could be a source of, or inspiration for, (1) new pharmacological agents and strategies designed to manipulate therapeutically connective tissue mechanical properties and (2) new composite materials with biomedical applications.

Journal of Zoology, 1992

The oral arm plates of the brittlestar Ophiura ophiura L. are connected to lateral arm plates at ... more The oral arm plates of the brittlestar Ophiura ophiura L. are connected to lateral arm plates at distal and proximal ligamentous junctions. The distal junction is mobile and is disrupted during arm autotomy; the proximal junction is more rigid and does not participate in autotomy. Aspects of the morphology and mechanical properties of the distal and proximal oral arm plate ligaments have been investigated in order to determine if their tensility is under physiological control. By means of creep tests it was found that elevation of the external potassium (K+) ion concentration causes a decrease in the viscosity of the distal ligament which is either transient or continues until rupture intervenes. In forced vibration tests the distal ligament often shows a biphasic stiffening then softening response to excess K - ions. Anaesthetics block the softening phase but enhance the stiffening component of this response. This ligament is also softened by repetitive electrical stimuli but stiffened by excess calcium ions and by acetylcholine. The proximal ligament appears to have the capacity for only transient changes in mechanical properties. Both ligaments are penetrated by the processes of juxtaligamental cells whose perikarya are arranged in clusters innervated by hyponeural nerves. These cells are thought to modulate the interfibrillar cohesion of the ligaments. It is concluded that the distal and proximal ligaments are mutable collagenous structures which in their stiffened condition help to maintain arm posture without the need for continuous muscular activity, and that at autotomy the distal ligament undergoes a profound loss of tensile strength which facilitates arm detachment.

Zoomorphology, 1992

The compass depressors are bands of soft tissue which connect the compass ossicles of the echinoi... more The compass depressors are bands of soft tissue which connect the compass ossicles of the echinoid lantern to the inner edge of the test. They are essentially ligaments with on one side a thin layer of muscle cells. The ligamentous component consists mainly of a parallel array of collagen fibrils with interspersed 12 nm microfibrils. The most notable cellular constituents are granule-containing cell bodies and their processes which resemble the juxtaligamental cells that have been found in all echinoderm mutable collagenous tissues and which may control the tensility of these tissues. The muscle cells occupy about 8% of the total cross-sectional area of the compass depressor and are located in a richly innervated pseudostratified myoepithelium. When subjected to constant low loads in creep tests the compass depressor stretches to a fixed length beyond which there is no further extension. The length at this creep limit coincides with the maximum length to which the compass depressor is stretched by natural movements of the intact lantern. Stress-strain tests show that treatment with 1 mM acetylcholine or 100 mM K+ ions can increase reversibly the stiffness of the compass depressor to an extent that cannot be due to contraction of the myoepithelium, suggesting that the mechanical properties of the ligament are under physiological control. Tension-length data on the myoepithelium suggest that it generates a maximum active tension when the compass depressor is stretched to the creep limit. The implications of these results for the function of the compass depressors are discussed.

Zoomorphology, 1987

In the arm of the ophiuroid Ophiocomina nigra the intervertebral muscles are linked to the verteb... more In the arm of the ophiuroid Ophiocomina nigra the intervertebral muscles are linked to the vertebral ossicles by tendinous connective tissue fibres. When an arm autotomizes, rupture of the tendons at one end (the autotomy insertion) permits each muscle in the autotomizing segment to separate cleanly from an ossicle while its other attachment (the non-autotomy insertion) remains intact. The anatomical relations, composition and function of the tendons were investigated by histochemical, electron microscopical and experimental methods. The tendons consist of a carbohydrate-rich secreted collagen derived from the basal lamina of the muscles. At autotomy their rupture is preceded and facilitated by an increase in extensibility, which represents the first evidence for variable tensility in an echinoderm connective tissue not composed of interstitial collagen. Granule-containing juxtaligamental cell processes are associated with the tendons of the autotomy insertions but are absent from the non-autotomy insertions. There appears to be widespread release of granules from these processes at autotomy. The results of a simple experiment implicate the juxtaligamental cells in the control of tendon extensibility and a possible mechanism for this control is presented.

Invertebrate Biology, 2009

Abstract. The ophiuroid Amphipholis kochii is able to detach its central disc from the underlying... more Abstract. The ophiuroid Amphipholis kochii is able to detach its central disc from the underlying oral frame in response to external stimuli. In this article we supply new observations on the microanatomy and ultrastructure of the autotomy plane, and of the juxtaligamental system which is believed to bring about connective tissue changes that underpin the detachment process. We correct previous confusion over the innervation of juxtaligamental nodes involved in disc autotomy, provide evidence that juxtaligamental cells are a population of specialized nerve cells, and present observations on changes in the ultrastructure of juxtaligamental cells during autotomy, which support the view that they are responsible for connective tissue disruption.

Zoology, 2014

Although sponges are still often considered to be simple, inactive animals, both larvae and adult... more Although sponges are still often considered to be simple, inactive animals, both larvae and adults of different species show clear coordination phenomena triggered by extrinsic and intrinsic stimuli. Chondrosia reniformis, a common Mediterranean demosponge, lacks both endogenous siliceous spicules and reinforcing spongin fibers and has a very conspicuous collagenous mesohyl. Although this species can stiffen its body in response to mechanical stimulation when handled, almost no quantitative data are available in the literature on this phenomenon. The present work was intended to quantify the dynamic response to mechanical stimulation both of intact animals and isolated tissue samples in order to evaluate: (i) the magnitude of stiffening; (ii) the relationship between the amount of stimulation and the magnitude of the stiffening response; (iii) the ability of the whole body to react to localized stimulation; (iv) the possible occurrence of a conduction mechanism and the role of the exopinacoderm (outer epithelium). Data on mesohyl tensility obtained with mechanical tests confirmed the difference between stimulated and non-stimulated isolated tissue samples, showing a significant relationship between ectosome stiffness and the amount of mechanical stimulation. Our experiments revealed a significant difference in tensility between undisturbed and maximally stiffened sponges and evidence of signal transmission that requires a continuous exopinacoderm. We also provide further evidence for the presence of a chemical factor that alters the interaction between collagen fibrils, thereby changing the mechanical properties of the mesohyl.

Invertebrate Reproduction & Development, 2012

Echinoderms have been used often as experimental models in developmental biology and evolutionary... more Echinoderms have been used often as experimental models in developmental biology and evolutionary biology studies. Numerous data on echinoid and asteroid development are available, whereas little is known about crinoid larval biology. This contribution focussed on the life cycle of the Mediterranean feather star Antedon mediterranea. Light and electron microscopy were used to characterize, in detail, the morphology and behaviour of the main larval stages. Similarities and differences with respect to what is already known for other crinoids, and echinoderm species, were explored. In view of the importance of serotonin during settlement and morphogenesis, analyses of the distribution of this molecule were carried out on swimming larvae. Immunolabelling results suggested a role for serotonin in A. mediterranea development, underlining the ancestral importance of this conserved neurotransmitter in deuterostome evolution.

Zoomorphology, 2005

This paper provides the first detailed account of the histological and ultrastructural organisati... more This paper provides the first detailed account of the histological and ultrastructural organisation of an echinoderm ligament that is non-mutable. Each of the five compass ossicles on the aboral side of the lantern of regular echinoids is linked to an underlying rotular ossicle by a compass-rotular ligament (CRL). The structure and anatomical relations of the CRL of Echinus esculentus L. were examined by light microscopy and scanning and transmission electron microscopy, and its responsiveness to neuroactive agents was observed in stress relaxation tests. The CRL consists of (1) thick collagen fibres that form an outer crossed fibre lattice and an internal system of parallel suspensory fibres and (2) regions composed mainly of bundles of ca. 12 nm microfibrils. The CRL is sparsely cellular, most cell bodies belonging to heterogeneous vesicle-containing cells that undergo apoptosis-like cytoplasmic fragmentation and produce linear aggregations of cell fragments. Coelothelia investing the CRL show intense secretory activity reminiscent of lamellar body production by mammalian mesothelia and are the source of bundles of cell processes that penetrate deeply into the CRL, branch sparingly and terminate between the thick fibres. Isolated CRL preparations are unresponsive to seawater containing 1 mM acetylcholine or 100 mM K+, but show a transient increase in stress relaxation rate when treated with 0.56 M KCl. The effects of solutions of other alkali metal chlorides suggest that the latter response is due to the direct action of KCl on extracellular components of the CRL and is not nervously mediated.

Journal of The Marine Biological Association of The United Kingdom, 2010

As well as acting as a neurotransmitter, serotonin is also involved in morphogenetic signalling d... more As well as acting as a neurotransmitter, serotonin is also involved in morphogenetic signalling during crucial phases of manydevelopmental and regenerative processes such as cleavage, migration and differentiation. Echinoderms display nervedependentregenerative phenomena and serotonin is one of the main neural regulatory factors that have been identifiedin them. The present work was designed to investigate the broad-spectrum involvement of this molecule

Zoomorphology, 1998

Certain components of the jaw apparatus, or lantern, of regular sea-urchins form a ’compass syst... more Certain components of the jaw apparatus, or lantern, of regular sea-urchins form a ’compass system’ the function of which has still to be established. This system includes ten compass depressors (CDs) which connect the compass ossicles to the inner edge of the test. Previous studies focused on the CDs of euechinoid sea-urchins. This paper provides the first detailed account of the organization and mechanical behaviour of the CDs of a cidaroid sea-urchin, Stylocidaris affinis. The outermost layer of its CDs is a coelothelium comprising apical peritoneocytes, sparse subapical myocytes and two types of granule-containing cells. The central core of the CD is dominated by longitudinally orientated collagen fibrils arranged in bundles surrounded by networks of beaded microfibrils. Myocytes are scattered throughout the core and are always surrounded by a basal lamina which usually encloses the same two types of granule-containing cells observed in the coelothelium. Each CD is attached to the outer coelomic septum by a mesentery, both the connective tissue and coelothelia of which lack myocytes and granule-containing cells. From data on the relationship between the vertical position of the lantern and the passive and active forces developed by intact CD sets, it appears that the CDs resist elevation of the lantern above its ’resting position’ and that they develop a maximal contractile force when their length corresponds to that at the resting position. The connective tissue of the CDs has the capacity to undergo nervously mediated changes in stretch resistance, although this is expressed more weakly than in the euechinoid CDs. These results are related to current views on the physiological role of the compass system.

Italian Journal of Zoology, 1994

The peristomial membrane is an area of flexible body wall which connects the test to the lantern ... more The peristomial membrane is an area of flexible body wall which connects the test to the lantern or masticatory apparatus of regular sea-urchins. The peristomial membrane of Paracentrotus lividus was examined by various light microscopical techniques and by scanning and transmission electron microscopy, and its mechanical properties were investigated by load-deformation tests. Attention was focused on the collagenous dermis which consists mainly of crossed-fibre arrays arranged in three histologically distinct sublayers. This microarchitectural arrangement gives rise to nonlinear load-deformation characteristics: when subjected to vertical deformation such as would occur during lantern protraction, the peristomial membrane shows firstly low stiffness and then high stiffness phases. The response of the peristomial membrane to chemical agents suggests that the tensile properties of the dermis are under physiological control. Our results indicate that the collagenous fibres of the dermis belong to separate populations whose stiffness can be adjusted differentially to meet changing functional demands on the peristomial membrane.

Journal of Experimental Biology, 2010

The crinoid echinoderm Antedon mediterranea autotomises its arms at specialised skeletal joints k... more The crinoid echinoderm Antedon mediterranea autotomises its arms at specialised skeletal joints known as syzygies that occur at regular intervals along the length of each arm. Detachment is achieved through the nervously mediated destabilisation of ligament fibres at a particular syzygy. The aim of this investigation was to identify neurotransmitters that are involved in the autotomy response. Physiological experiments were conducted on isolated preparations of syzygial joints, which can be induced to undergo autotomy-like fracture by applying stimulatory agents such as elevated [K(+)](o). Initial experiments with elevated [K(+)](o) showed that the autotomy threshold (the minimum amount of stimulation required to provoke autotomy) is lowest in syzygies at the arm base and rises distally. Of a range of neurotransmitter agonists tested, only l-glutamate invoked syzygial destabilisation, as did its analogues l-aspartate, alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) and kainate, but not l-(+)-2-amino-4-phosphonobutyrate (l-AP4) or N-methyl-d-aspartate (NMDA). The implication that l-glutamate stimulates syzygial fracture through AMPA/kainate-like receptors was supported by the finding that the action of l-glutamate was inhibited by the AMPA/kainate receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX). Acetylcholine depressed the response of syzygial preparations to l-glutamate, suggesting a possible mechanism by which the autotomy threshold could be varied constitutively and facultatively. An immunocytochemical method employing a polyclonal antibody against l-glutamate conjugated to glutaraldehyde revealed l-glutamate-like immunoreactivity in all components of the putative neural pathway controlling the autotomy reflex, including the epidermis, brachial nerve, syzygial nerves and cellular elements close to the syzygial ligaments. We conclude that it is highly probable that l-glutamate acts as an excitatory neurotransmitter in the activation of arm autotomy in A. mediterranea.

Marine Biology, 2000

Arm damage is a widely reported but superficially investigated aspect of the biology of the star... more Arm damage is a widely reported but superficially investigated aspect of the biology of the starfish Asterias rubens L. In the present study, the incidence of arm damage was surveyed in populations of A. rubens at two sites in the Firth of Clyde, Scotland, and three sites in Gullmarsfjorden, Sweden. The mean (±SD) incidence across all sites of individuals with basal arm damage (resulting from detachment at the basal autotomy plane) was 19.69 ± 8.86%, the incidence of those with distal arm damage (resulting from amputation at more distal levels) was 7.74 ± 10.01%. The mean incidence of arms with basal damage was 5.28 ± 4.12%, of those with distal damage 1.83 ± 2.45%. There was a significant negative correlation between size and the incidence of basal damage at all but one site, but no significant correlation between size and distal damage at any site. Mechanical tests on specimens of the aboral body wall from the basal region of the arm (which included the autotomy plane) and from a more distal region revealed that with increasing body size there was a significant increase in yield stress, ultimate stress and Young's modulus (stiffness) but no significant change in yield strain and ultimate strain. There was no significant difference between the relationships for basal and distal specimens. It is hypothesised that in larger individuals increased mechanical toughness replaces autotomy as an effective antipredator strategy. Using two methods to induce autotomy, a significant positive correlation between size and the delay between the onset of stimulation and arm detachment was found; this may represent a size-related decline in the efficiency of the autotomy mechanism through the relaxation of selection pressure. Since size is an unreliable indicator of age in A. rubens, the trends identified herein can be interpreted only tentatively as age-associated phenomena.