Morphological Adaptations of Intestinal Helminths

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866 THE JOURNAL OF PARASITOLOGY, VOL. 77, NO. 6, DECEMBER 1991endoderm or digestive tract and with no survivingfree-swimming or ectoparasitic ancestralforms, von Ihering reasoned that they are themost ancient of the parasitic worms." From suchreasoning it would be concluded that the tapewormsof fishes are more ancient and thereforebetter adapted to their hosts than those of othervertebrates. Indeed, some of the best examplesof morphological adaptation to the intestinal microenvironmentmay be seen in the cestodes ofelasmobranchs.MORPHOLOGY OF THE VERTEBRATEINTESTINEAccording to Crompton (1973), "The most obviousdifferences between the histology of the[intestinal] tracts of different vertebrates occurin the mucosa. The extensions and ramificationsof the mucosa of the small intestine are indicativeof the amount of absorptive and secretory activityand the amount of food available for the speciesof helminth which browse on the mucosa.The greatest development of the mucosa is seenin birds and mammals, where in addition to foldingthere may be as many as 40 villi per mm2 ofintestinal surface and 3,000 microvilli per epithelialcell per villus. It appears, therefore, thatpotentially more environments will be presentfor small helminths in the small intestines ofbirds and mammals than in those of fish, amphibians,and reptiles."Significant differences in mucosal structureamong members of the same genus also havebeen reported, as illustrated by Williams (1960)who compared histological sections of the spiralvalve of 3 species Raja, showing what the surfacewould look like to an observer in the lumen. Heattributed host specificity to the observation thatthe scolex appeared to interlock with mucosalfolds and villi.SITE SELECTIONMucosal architecture varies not only amongspecies, but also from region to region in thesame animal. Crompton (1973) concluded thatthe greatest degree of morphological variation isseen in the alimentary tracts of teleost fishes.Analysis of helminth distribution in the alimentarytract of the flounder demonstrated quiteclearly the spatial stratification of niches in theintestine occupied by the different species, andit revealed patterns of seasonal and age differencesin parasite distribution (MacKenzie andGibson, 1970).Interactive site selection by intestinal helminthshas been well documented for experimentalinfections of Hymenolepis diminuta andMoniliformis moniliformis (=Moniliformis dubius)in the rat (Holmes, 1973). Examining naturalinfections of the white sucker, Catostomuscommersoni, Grey and Hayunga (1980) foundthat the cestode Glaridacris laruei was displacedfrom its typical site in the posterior gut by largenumbers of the acanthocephalan Pomphorhynchusbulbocolli. From this observation they concludedthatthe habitat range of G. laruei is greater than had beenthought previously, and the fundamental niche of thisspecies appears necessarily broader than that of P. bulbocolli.Our data suggest that G. laruei is a "generalist"and P. bulbocolli a "specialist," at least with regard tospace (terminology of Colwell and Fuentes, 1975). Thespecialist is able to exclude the generalist either by moreefficient utilization of a critical resource or by someform of interference, while the generalist is capable ofestablishing in adjacent habitats.In this regard, it is certainly appropriate to viewa suitable mucosal topography as one of the criticalresources required by an intestinal parasite.Clearly, morphological adaptation has a bearingupon site selection, just as it had upon hostspecificity. Presumably the specialist, the wormthat is highly adapted to the topography of itspreferred site, will attach itself more efficientlyand be a better competitor. However, as demonstratedby G. laruei, there are times when beinga generalist is a better strategy. Intestinal helminthshave found success using both strategies.Their various approaches are described in detailin Crompton's (1973) review.MORPHOLOGICAL ADAPTATIONS OFPARASITESAs Crompton (1973) observed, "The presenceof nematodes in so many sites in the intestine isprobably related to their having an alimentarytract, and to the small size of many species whichis likely to facilitate the colonization of numerousnooks and crannies inaccessible to acanthocephalansand cestodes." Specialized attachment organsdid not evolve in nematodes and their feedingapparatus became adapted for burrowing andattachment whereas their digestive systems becamemodified to cope with the variety of materialsswallowed. Parasitic nematodes "feed ina variety of ways, many of these being independentof the host's digestive physiology" (Crompton,1973). The nematode cuticle plays an im-
HAYUNGA-MORPHOLOGICAL ADAPTATIONS OF INTESTINAL HELMINTHS 867portant role in protection, osmoregulation, andpossibly locomotion; its structure was describedin detail by Lee (1966).Digenetic trematodes have well developedventral suckers, facilitating attachment and enablingthem to browse on the mucosa. As suggestedby Crompton (1973), "the cellular debrisproduced during the constant renewal of the intestinalepithelium may be a major item in thediet of many trematodes, and the rapid epithelialturnover rate may explain, in part, how largepopulations of grazing trematodes can be supportedin the alimentary tract." The trematodetegument is arranged as a "sunken epidermis"consisting of a syncytial surface layer connectedby internuncial processes to subtegumental cytonslying below the layer of cuticular muscles;the syncytium contains prominent spines that"probably assist the parasite in retaining its positionin the host" (Lee, 1966). The tegumentalsurface of the bloodstream-dwelling Schistosomatidaeis modified by the presence of a heptalaminatesurface membrane that presumablyplays a role in protecting helminths bathed in asea of immunoglobulins (Hockley, 1973). Uptakeof nutrients by trematodes can occur boththrough the gut and tegument; however, the relativenutritional roles of these surfaces in vivois not clear (Pappas, 1988).Strigeid trematodes utilize a complex adhesiveorgan to maintain attachment to the mucosa(Erasmus, 1977). Unlike the general tegumentcovering most of the worm's body, the tegumentof the adhesive organ is highly modified withspecialized invaginations, or pits, and lappets withdistinctive setae and lappet gland cells. As Erasmus(1969) reported,When the adult Apatemon becomes attached to themucosa of the host, a host tissue plug, consisting largelyof the intestinal villus divested of its mucosal epithelium,lies between the adhesive organ lobes. In thisway the inner face of each adhesive organ lobe comesinto very intimate contact with the host's lamina propria.Under the light microscope the association appearsto be so intimate that it is often impossible todistinguish precisely the extent of the parasite tegument.Proposed functions for the adhesive organs haveincluded adhesion to the host, the release of histolyticsecretions, and extracorporeal digestionand the absorption of nutrients; although supportedby little direct evidence, the concept ofthe adhesive organ having a "placental role" isan intriguing notion (Erasmus and Ohman, 1963;Erasmus, 1977).Acanthocephalans are firmly anchored by theircharacteristic armed proboscis that embeds itselfinto the submucosa. Lacking a gut, they absorbnutrients through their trunk. The acanthocephalanbody wall is a complex syncytium, with numerouspores and canals, and several structurallydistinct layers, serving both a protective and absorptivefunction (Lee, 1966). Van Cleave (1952)suggested that the proboscis might absorb nutrientsdirectly from host tissues. But accordingto Crompton (1973) this possibility is not easilysupported because "the surface area of the proboscisis very small compared with that of thetrunk, and the fact that the proboscis often elicitsan inflammatory response, followed by the depositionof fibrous material, means that accessof nutrients to the proboscis is likely to be impeded."Of striking similarity to the strigeid adhesiveorgan are the tegumental modifications seen inthe acanthor stage of the the acanthocephalan M.moniliformis, as depicted by Crompton (1975).After penetrating the intestinal tissues of its invertebratehost, the cockroach Periplaneta americana,the acanthor becomes surrounded by hosthemocytes. Although by no means proven, thereis the visual suggestion that such surface amplificationmay serve to protect the parasite fromhost rejection by keeping the tegument properand the host cells apart.Because cestodes must obtain all of their nutrientsthrough the tegument, their surfaces havebeen among those most studied. As early as 1874,Schiefferdecker (1874) observed hairlike projectionson the tegumental surface of Taenia; suchprojections closely resembled the brush borderfound on intestinal epithelium. Using informationobtained from electron microscopic studies,Beguin (1966) drew the analogy between the cestodetegument and intestinal epithelium, and heenvisioned a distinction between the absorptivefunctions of the surface membrane and distalcytoplasm and the other functions of organellesfound more proximally. However, the fingerlikeextensions of the tapeworm's surface appear morecomplex than intestinal microvilli, as they consistof both a proximal, microvilluslike shaft, anda distal tapered spine. The term microthrix (plural,microtriches) was proposed by Rothman(1959) to describe this surface modificationunique to cestodes.The primary function of the microtriches was
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Morphological Adaptations of Intestinal Helminths

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