Concluding Comments

Our review is the first attempt to draw together information about use of adhesion, in the sense of attachment by chemical means via a thin layer of adhesive material, by symbiotic or parasitic platyhelminths, or indeed by any parasite group, to a host organism. Adhesion by adhesins (i.e. surface molecules known from, and characterized in, some bacteria and protists that invade host cells) is an active, but currently separate, research field (e.g. Alderete, 1999; Kennett et al., 1999). Future studies may indicate whether there are similarities in the molecular interactions between these invaders and their host cells and the bioadhesives secreted for attachment to their host's surfaces by, for example, the flatworms reviewed here.

The ubiquity of adhesion in nature was referred to in Section 2. The burgeoning discipline of bioadhesion is testimony to the innate curiosity, interest and importance placed on understanding how adhesion in nature occurs. Other outcomes from bioadhesion studies not only include attempts to replicate in the laboratory or in industry methods of producing such tenacious natural adhe-sives which are known for their toughness (B.L. Smith et al., 1999), but also embrace development of methods to prevent some organisms from adhering (i.e. production of antifoulants). Marine invertebrates are a particularly rich source of natural adhesives and, as Flammang (1996) phrased it so clearly, 'adhesion is a way of life in the sea'. Many marine invertebrates with a benthic or interstitial lifestyle have evolved various organs, organelles and/or secretions for adhesion to different substrates. Generally, however, these surfaces are non-living (i.e. abiotic). We have emphasized that some parasitic organisms, many from marine vertebrate hosts, have developed mechanisms by which they can adhere to a living (i.e. biotic) surface. We believe that adhesion to living surfaces (= tissue adhesion; Section 3.4) represents an exciting extension to the arena of bioadhesion.

Tissue adhesion has important implications for the biology of organisms, especially parasites such as monogeneans and animals like some barnacles, that have evolved effective systems to adhere to epithelia. Substrates such as vertebrate epithelia are moist, usually slimy and covered by a mucous layer and are equally as inhospitable as intertidal rocky zones and ship hulls, surfaces commonly occupied by invertebrates such as mussels and barnacles and subject to strong shear forces from tidal action. Epidermis could, perhaps, be considered more hostile than abiotic substrates in the ocean because they may contain elements of the immune system. We hope the concept of tissue adhesion will provide a catalyst for further study in parasitology. These studies should include: the potential importance of adhesives in host- and site-specificity; the role of adhesives in provoking an immune response from a host; how attachment by adhesives may contribute to the co-evolutionary arms race between parasites and hosts (Whittington et al., 2000a). Host- and site-selection by parasites based on adhesive-host substrate recognition may resemble the phenomenon of 'habitat selection' (i.e. choice of favourable versus unfavourable, but inert, surfaces) by pelagic larvae of free-living, benthic marine invertebrates (Hadfield, 1998; Whittington et al., 2000a).

Permanent adhesion to abiotic substrates by marine organisms such as mussels and barnacles is achieved principally by proteinaceous secretions that contain little or no carbohydrate (Section 9). The chemistry of temporary adhesives for attachment to abiotic substrates is poorly characterized (Flammang, 1996), but studies on limpets and starfish indicate that complexes of proteins and carbohydrates are common (Section 9). A.M. Smith et al. (1999) discovered that the limpet, Lottia limatula (Mollusca: Gastropoda), is able to change the amount of protein and carbohydrate in its single adhesive secretion and this difference in proportion changes its properties to allow either gliding or adhesion. Similarly for starfish, the ability to vary the ratio of acid mucopolysaccharides to protein across taxa (Flammang, 1996) may alter the strength of the adhesive. In comparison with these marine macroinverte-brates, the chemistry of adhesives in platyhelminths is virtually unknown, largely because of their small size. Indications on present evidence suggest strongly, however, that proteins and, in some cases carbohydrates, are also important in flatworm adhesives. The duo-gland system of turbellarians has proteinaceous and glycan components and is perhaps a glycoprotein (Tyler, 1988). In monogeneans (Section 5), anterior adhesive secretions are proteins (Hamwood, Cribb, Halliday, Kearn and Whittington, unpublished data) and posterior cements are lipoprotein (Rand et al., 1986). Secretions implicated in adhesion among cestodes (Section 6) are mucopolysaccharides in an oncosphere (Kashin, 1986), and glycoproteins in a metacestode (Brockerhoff and Jones, 1995) and in adults (McCullough and Fairweather, 1989; Stoitsova et al., 1997). The posterior adhesive from the rosette organ in a gyrocotylidean has been characterized as a mucoprotein (Lyons, 1969).

For turbellarians (Section 4) in which there is usually more than one secretory type in their adhesive systems, there is no clear information about possible interactions or chemical differences between different components despite ultrastructural studies of many taxa. In the monogeneans (Section 5), anterior adhesive secretions of only 15 species from five families (Table 1) have been studied in detail. There is usually more than one secretory type released anteriorly by monogeneans and several hypotheses have been proposed about their possible interactions (Section 5.2.2(e), p. 157). Most information is available for the capsalid monogenean, Entobdella soleae, from work by Kearn and Evans-Gowing (1998). They presented evidence to suggest that two secretory types interact to produce the adhesive and some evidence to indicate that the specialized tegument of the anterior adhesive areas may be the agent responsible for detachment (Kearn and Evans-Gowing, 1998). There is clearly a need to investigate anterior adhesion in more monogenean species from a range of parasite families, and from a diversity of host taxa, to determine more about interactions between different secretions and how detachment mechanisms operate. Future studies to contribute information to fill some of these gaps in our knowledge about platyhelminth adhesion, especially the tissue adhesion displayed by monogeneans, provide significant but exciting challenges in parasitology and in the sphere of bioadhesion.

Despite the apparent similarities in the chemical composition of adhesives highlighted above among many marine invertebrates from different taxa, Tyler (1988) asserted that a variety of polymers could act as natural adhesives. By focusing on the so-called duo-gland adhesive system reported from various marine invertebrates (e.g. Tyler, 1976; Hermans, 1983), Tyler (1988) considered that a functional comparison, including secretion chemistry, showed that variety was encountered. Tyler (1988) proposed that this variation demonstrated that there is no universal mechanism common to the adhesive systems in these different marine organisms and that any similarities between major invertebrate groups are due to convergence. Even within the so-called duo-gland organs of turbellarians, gastrotrichs and nematodes, functional differences (specifically different polymers) demonstrate convergent morphological similarity (Tyler, 1988). Determination of which secretions function as adhesives and which may serve other purposes such as detachment ('release' or 'de-adhesion' in other terminology) were cited by Tyler (1988) as difficulties to overcome. Many of these quandaries remain for future investigations on temporary adhesion by starfish and turbellarians and for tissue adhesion by monogeneans.

Structural similarities across the variety of glandular adhesive systems reviewed here relate to the activity of secretory cells across the eukaryotes. Common cellular components and structural architecture include: unicellular gland cells containing Golgi complexes and rough endoplasmic reticulum; microtubules around some secretory bodies during their formation; microtubules that line the neck or duct endings; short microvilli on the surface of the organism close to where ducts open. Evidence for the importance of microtubules as cellular 'motors' for organelle movement and membrane traffic is increasing (Goodson etal., 1997). This supports earlier suggestions that microtubules may play a role in transport of vesicles containing secretory material from Golgi apparatus during formation of turbellarian rhabdites (Lentz, 1967) and rod-shaped bodies in monogeneans (El-Naggar and Kearn, 1980). El-Naggar and Kearn (1980) discussed other possible roles for microtubules. For those surrounding forming secretory bodies, it was suggested the microtubules may orientate the rods within the lumen of the gland ducts to form parallel bundles, whereas for those lining duct terminations, it was suggested that if microtubules are contractile, they may assist secretion of bodies to the exterior (El-Naggar and Kearn, 1980). Most of these suggestions appear likely and probably explain the apparent widespread presence of microtubules in cells with secretory activity across a diversity of taxa.

The morphological similarity in adhesive systems between different phyla is very likely due to convergence: in the marine environment, for example, attachment to a variety of substrates is probably an adaptive feature (Tyler, 1988). Our review, however, has focused on adhesives in a single phylum, the Platyhelminthes, and there have been several discussions about whether there is homology between the adhesive glands of different flatworm groups, e.g.

between turbellarians and monogeneans (El-Naggar and Kearn, 1983; Rees, 1986; Kearn and Evans-Gowing, 1998; Cribb etal, 1998) and between all flat-worm groups (Ehlers, 1985; Rohde, 1990; Xylander, 1990; Jondelius, 1992; Littlewood et al., 1999). There is general agreement that turbellarian Rhabditophora are characterized by lamellar rhabdites (Rohde, 1990; Rieger et al., 1991; Littlewood et al., 1999) and that turbellarian Rhabditophora (see Rohde, 1990; Littlewood et al., 1999) and Macrostomida (see Littlewood et al., 1999) have duo-gland adhesive organs consisting of one anchor cell and two types of gland cells. Rohde (1986) was of the opinion that further studies were required to assess homology or otherwise among anterior gland cells in the parasitic platyhelminths.

Ehlers (1985) regarded the anterior adhesive systems of monogeneans and the adhesive systems of turbellarians as fundamentally and structurally different and concluded that the duo-gland system of rhabditophoran turbellarians and the anterior adhesive systems of monopisthocotylean monogeneans have arisen convergently and are, therefore, analogous, not homologous. For further discussion, see Jondelius (1992) and Kearn and Evans-Gowing (1998). We consider that caution and further study is required before Ehlers' conclusion can be stated with any certainty. To argue against Ehlers' (1985) hypothesis of convergence, the duo-gland system of turbellarians and the anterior adhesive areas of most monopisthocotylean monogeneans have separate secretions emerging via ducts that pass through a surface cell or syncytial layer of cytoplasm provided with microvilli. After further study, it is possible that each of these systems may be shown to be the same functionally for it must be remembered that Tyler's (1976, 1988) explanations for the mode of action of the duo-gland system in turbellarians is based on speculation (Sections 3.5, 4.4, 4.10 and 9). Furthermore, some differences between the adhesive systems of these taxa may be expected should monogeneans have inherited their adhesive systems from turbellarian ancestors. In our opinion, homology or otherwise of the duo-gland system of turbellarians and the anterior adhesive areas of monopisthocotylean monogeneans remains unresolved.

It is intriguing that a major secretory product of the Turbellaria, the rhabdite (Section 4.3), known to have adhesive properties among temnocephalans (Section 4.6), bears a close resemblance in shape, if not in structure (compare Sections 4.3, 5.2 and Table 1), to rod-shaped bodies secreted by one type of anterior adhesive gland in monopisthocotylean monogeneans. While further study of the ultrastructure of monogenean rods is likely to be fruitful, rhabditophoran rhabdites appear to be more complex than monogenean rods. Llewellyn (1965) proposed that ancestral monogeneans arose from free-living rhabdocoel-like ancestors and, therefore, resemblance between the adhesive secretions and systems of monogeneans and turbellarians may reflect common ancestry. For further discussion on this, see El-Naggar and Kearn (1983). However, it remains to be determined whether the shape of these 'rhabdiform'

bodies reflects a phylogenetic link (see above) or whether it has some functional significance. Further studies on possible interactions between different secretory types may clarify this.

The continued success of a diversity of flatworms owes much to the persistent development and refinement of their attachment by adhesion, which has assumed critical importance in their biology, whether they live in the interstitial environment, or subsist as symbionts or parasites. The range of adhesive systems in platyhelminths extends beyond the duo-gland system of turbellarians (Section 4.4) and the anterior adhesive areas of monopistho-cotylean monogeneans (Section 5.2). It includes the 'frontal organ' and 'frontal glands' of free-living turbellarians (Section 4.5), various glands described from symbiotic turbellarians (e.g. anterior glands in Pterastericolidae, possibly frontal glands in graffillids and other secretions, including rhabdites, from temnocephalan tentacles; Section 4.6), gland cells from the posterior end of monopisthocotylean monogeneans (Section 5.3) and putative adhesives secreted by some cestode stages (Section 6). Many of these systems may have evolved independently, especially some of the diversity of adhesive systems reported among turbellarians (Section 4). Haptor adhesive glands in some monogeneans have probably evolved more than twice (in microbothriids, anoplodiscids and in at least two genera of dactylogyrids; Section 5.3).

It is surprising that the diversity of characters known from the anterior ends of monogeneans have not been used in phylogenetic assessments based on morphology (e.g. Boeger and Kritsky, 1993, 1997, in press) and we will redress this situation in the future. The diverse morphology of the anterior adhesive areas and the number, ultrastructure and chemistry of the different secretory types seem likely to be especially informative.

Xylander (1990) considered the structure and function of the anterior glands of the lycophore larva of Gyrocotyle urna (Gyrocotylidea; Section 6.3). On comparing these glands with those of the larvae of other parasitic platyhelminths (the Neodermata of Ehlers, 1985), Xylander (1990) concluded that a clear correspondence between glandular systems of different types of larvae of the Neodermata was not possible. Ten years after this statement by Xylander (1990), we have reached the same conclusion following the present detailed review based on evidence from larvae and adults. However some uncertainties in our knowledge have been addressed. Xylander (1990) wrote that larval glands of all Neodermata degenerate after infection of the host and that glands in many postlarvae arise de novo and are not related to glands observed in larvae. Chisholm and Whittington (1996b) have since proposed the possible homology of gland cells in the oncomiracidium and adult of Heterocotyle capri-cornensis (Monogenea: Monopisthocotylea: Monocotylidae). Other similar gland homology is likely to exist more broadly across the Neodermata.

Efficient methods of temporary adhesion in turbellarians and monogeneans probably reflect the importance of mobility to these flatworms that have relatively simple life cycles and occur mostly on external surfaces, whether inert particles and substrates or living epithelia. For cestodes and digeneans, however, the complexity of their indirect life cycles places considerable and different demands on all stages. Whether an active infective larva, a larval stage requiring passive consumption by an intermediate host or a juvenile (e.g. a metacestode or a metacercaria) inside an intermediate host waiting to be consumed, there is often less, or no, requirement for anterior adhesive glands. Instead, the emphasis for infective stages of the endoparasitic flatworms is primarily for penetration into a host or penetration through various tissues from the gut when eaten by an intermediate host. Section 6 on cestodes and Section 7 on digeneans review the diversity of gland cells at the anterior end of larval, juvenile and adult stages, but accounts of unequivocal adhesive secretions are relatively rare. It is possible, however, that use of adhesives in cestodes and flukes may have been overlooked. A conspicuous array of anterior glands are present whose primary purpose appears to be to secrete histolytic secretions for penetration into, or escape from, hosts, but whether evolution of these glands for this range of tasks is independent or not is unknown, and more studies are required.

In adult cestodes and digeneans, there is the general perception that these endoparasitic flatworms have considerably less need for mobility. Nevertheless, tapeworms are known to migrate along the gut (Kearn, 1998) and digeneans can move by looping using the oral and ventral sucker (e.g. Sukhdeo et al., 1988). Adhesive secretions from the scolex of some adult eucestodes is reported and it seems likely that this phenomenon has arisen independently in different orders, although further research is necessary. It is possible that some digeneans such as the bucephalids have an increased reliance on adhesives, but this also requires confirmation. Even the efficient and large ventral attachment organ of aspidogastreans (Figure 23) is reported to be supplemented by secretions proposed to have an adhesive function (Timofeeva, 1972). Clearly, there is a need for a critical assessment after further investigation of the presence, extent, characteristics and characterization of secretions, using ultrastructural and chemical methods, among the endoparasitic platyhelminths.

Studies will continue to examine adhesion in the more easily accessible and readily observable ectoparasitic monogeneans. It will be of interest to compare the chemistry of the kinds of adhesives used by different platyhelminths for tissue adhesion to external epidermal surfaces (e.g. fish skin) by monogeneans with the less common (?) tissue adhesion by tapeworms and flukes for attachment to the lining of the vertebrate intestine and its outgrowths. We predict that convergence in the chemistry of their adhesives is most likely because these different but related parasites face similar problems of attachment to host tissue. One difficulty that investigators will face in studies of the chemistry of flatworm adhesives is obtaining sufficient quantities of material on which to work.

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