Morphological Adaptations of Intestinal Helminths

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

868 THE JOURNAL OF PARASITOLOGY, VOL. 77, NO. 6, DECEMBER 1991thought to be surface amplification, as the efficientabsorption of nutrients by the tegument wasessential for helminths that had no gut. Microtricheswere also implicated in protection fromthe host (Morseth, 1966; McVicar, 1972), anchoring(Rothman, 1963; Mount, 1970; Hayungaand Mackiewicz, 1975), and locomotion(Rothman, 1963; Berger and Mettrick, 1971).Other suggestions have included the possibilitythat the microtriches might anchor the parasiteby interdigitating with the intestinal microvilli(Rothman, 1963) or that the spines might actlike cilia to facilitate absorption by agitating themicrohabitat and thus recirculating the intestinalcontents (Rietschel, 1935). There is strong evidencethat "membrane digestion" (adsorption ofdigestive enzymes by the surface membrane) occursin cestodes (Smyth, 1972) and that contactstimulus between the mucosa and the scolex maytrigger strobilization and development (Smyth,1969a); however, the role of the microtriches inthese processes is not clearly defined.Some very revealing clues about microthrixfunction were obtained from observations madeby Braten (1968) who carefully compared thesurfaces of larval and adult specimens of Diphyllobothriumlatum. As a result of detailedmeasurements from electron micrographs, heobserved that both the number and size of thetegumental microtriches of D. latum adults weresignificantly greater than those of the plerocercoidstage. This represented a significant surfacearea amplification that could be correlated withthe increased metabolic demands of transitionfrom the intermediate to the definite host. However,his measurements further revealed that mostof the growth in the microtriches occurred in theproximal shaft whereas the size of the distal spineremained relatively constant. From this he concludedthat the shaft of the microthrix was involvedin nutrient absorption but that the spinemust have some other function, perhaps protectionor anchoring. An anchoring function for themicrothrix spine was given further support bythe work of Mount (1970) who showed that therostellar hooks of Taenia crassiceps appear todevelop directly from microtriches with unusuallylarge spines.The greatest amount of variation in attachmentorgans is seen in cestodes, particularly thoseof fishes. The rosette of the monozoic cestodariansappears to be a delicate holdfast organwhereas the larger, strobilated eucestodes requirethe stronger attachment afforded by a scolex. Thecestodes of elasmobranchs display an impressivevariety of holdfast modifications, with elaboratebothridia and a fingerlike projection of the scolex,the myzorhynchus, that penetrates the mucosato afford an even firmer anchoring. As illustratedby Williams et al. (1970), the scolexoften appears tailored for an exact fit with themucosal villi of its host. "Williams dispelled thesuggestion that the scolex subsequently grows tofit in with the host's mucosa after the establishmentof infection by stressing that the main featuresof scolex morphology are present at an earlydevelopmental stage. In a young specimen ofEcheneibothrium sp. the scolex is almost identicalin size and form with that of an adult specimen"(Crompton, 1973).In his examination of the parasite-host interfaceof 3 tetraphyllidean species, McVicar (1972)observed that the tegument of the bothridial rimof Acanthobothrium quadripartitum was attachedso firmly that parts of the host mucosalcells appear to be pulled apart, leaving noticeableintracellular spaces. Examination of the sites ofbothridial attachment for the other species revealeda breakdown of the host intestinal microvilliand the accumulation of membrane-boundosmophilic material in the host cells. In Echeneibothrium,species of which possess a myzorhynchus,the intestine showed signs of severedamage at the site of penetration. Both the presenceof tegumental microtriches with well developedproximal shafts and the high level ofalkaline phosphatase activity in the tegument ofthe myzorhynchus, together with the obviousdegradation of host tissue, lend credence toSmyth's (1969b) suggestion of a "placental role"for the attachment organs of at least some cestodespecies.HOST RESPONSE TO THE PARASITEFor the most part the host response to intestinalhelminths involves a typical inflammatoryreaction (see review by Befus and Bienenstock,1982). Histological changes in the mucosa followinginfection may include goblet cell hyperplasia(Ackert et al., 1939), hyperplasia of thepaneth cells (Roberts-Thomson et al., 1976),villus atrophy and crypt hyperplasia (Symons,1965; Manson-Smith et al., 1979), and the typicalhistopathological changes associated with anintestinal granulomatous response (Jones andRubin, 1974).McVicar (1972) had concluded that "variationin the degree of damage inflicted by the bothridia

HAYUNGA-MORPHOLOGICAL ADAPTATIONS OF INTESTINAL HELMINTHS 869FIGURE 1. Section through a nodule of Hunterellanodulosa, showing loss of epithelium at the opening ofthe nodule and hyperplasia of the submucosal tissue.Note how the posterior part of the worm extends intothe lumen of the gut (plastic section, toluidine blue).(From Hayunga and Mackiewicz [1975], courtesy ofPergamon Press.)of the tapeworms of R. naevus seems to dependpartly on the cestode's size, mode of attachmentand ability to move." The results of his examinationof the parasite-host interface of tetraphyllideanssuggested a strong relationship betweenscolex structure and intestinal damage.Around the same time as that study, Mackiewicz(1972) was independently asking similar questionsabout caryophyllidean cestodes. Caryophyllideansdisplay considerable variation inscolex structure, ranging from the totally undifferentiatedanterior surface of Hunterella nodulosato species whose attachment organs includebothria, loculi, and terminal discs, each in variousdegrees of development. Furthermore, theirrestriction to cyprinid fishes should allow for directcomparisons of intestinal damage.Mackiewicz et al. (1972) reported that thegreatest degree of intestinal damage was observedfor those caryophyllidean species withpoorly developed attachment organs. Monobothriumingens, H. nodulosa, Monobothrium ulmeri,and Biacetabulum biloculoides were eachassociated with pronounced granulomatous reactions,resulting in the formation of conspicuousnodular lesions that in some cases containednecrotic material. The presence of an eosinophilic,perhaps mucoid, layer at the parasite-hostinterface, best seen in M. ulmeri, "varies fromspecies to species. It is generally absent wherethere is no tissue reaction and is most pronouncedin the nodules and other lesions." It isprobably a secretory product of the parasite; suchmaterial was suggested by Liu and Edward (1971)to function as an adhesive. In contrast, thosespecies with well developed, specialized holdfastorgans elicit little or no response; intestinal damageappears limited to compression of the villiand minor distortion of the shape of the crypts.This topic was pursued further by Hayunga(1977) who examined scolex structure of the mostundifferentiated species, H. nodulosa, at both thelight and electron microscopic levels. As shownin Figure 1, H. nodulosa is found in the anteriorgut, clustered within a nodular lesion characterizedby a loss of epithelium and extensive hyperplasiaof the submucosal tissue. Althoughlacking holdfast organs, worms are anchoredfirmly in the nodule and must be removed forciblyfor examination. When relaxed, the posteriorportion of the parasite extends into the lumenof gut.Electron microscopic examination of the tegumentof H. nodulosa revealed typical cestodemicrotriches covering the surface of the anteriorportion of the worm (Fig. 2). However, microtricheson the posterior surface were noteworthyin that they lacked the terminal spine (Fig. 3) andmore closely resembled the surface microvilli ofthe cestodarian Gyrocotyle urna as described byLyons (1969). These findings support earlier conclusionsthat the proximal shaft of the microthrixis primarily involved in the absorption of nutrients,whereas the spine assists in anchoring theparasite. However, as the crypt of the nodule isdevoid of host epithelium, any anchoring functionof the microtriches must be achieved bymeans other than interdigitation with intestinalmicrovilli (Hayunga and Mackiewicz, 1975). Lackof phosphatase activity on the scolex surfacewould be consistent with the notion that the absorptionof nutrients is restricted to the posteriorpart of the worm, and it suggests there may beregional differences in tegumental function (Hayunga,1979a). The idea of localized tegumentalactivity in flatworms was given further supportby experimental work on Schistosoma mansonireproductive behavior (Popiel and Basch, 1984).Light microscopic examination of the lesionassociated with H. nodulosa infection shows anarea of chronic inflammation and extensive infiltrationof lymphocytes. A prominent eosinophilicmatrix is found between the parasite andhost tissue. Tegumental microtriches are so firmlyattached to this matrix that often portions ofthe tegument are left behind when worms areforcibly removed from the nodule (Hayunga,1977, 1979b). Electron microscopic examination

870 THE JOURNAL OF PARASITOLOGY, VOL. 77, NO. 6, DECEMBER 1991Iul#lIIIHHII rlul1u1!111lt!1lllf!( A,t.A^Q1mI>71111101111 11i1I110111110111110111-11111111011 111-100 -,'0 -~IO.5jmEFGH. ..IFIGURE 2. Diagram of the tegumental arrangementin the neck region of Hunterella nodulosa. cm, circularcuticular muscles; er, endoplasmic reticulum; g, golgi;gly, glycogen; lm, longitudinal cuticular muscles; m,microtriches; mit, mitochondrion; n, nucleus; no, nucleolus;r, rod-shaped bodies; v, vesicles (from Hayunga[1977]).reveals the eosinophilic matrix to be a secretoryproduct of the scolex, as large vesicles originatingfrom frontal glands were observed to be transportedtranstegumentally to release their contentsat the parasite-host interface; the failure ofthe frontal glands to stain for proteolytic enzymessuggests that the secretion is not lytic butrather adhesive in nature (Hayunga, 1979a,1979b). Because the frontal glands of H. nodulosaare better developed than those of othercaryophyllideans, they are very likely to play amajor role in attachment and penetration (Mackiewiczet al., 1972). However, the actual functionof both the frontal glands and the Faserzellen or"neck cells" of caryophyllideans remains to bedemonstrated (Mackiewicz, 1972; Hayunga andMackiewicz, 1988).PARASITE EXPLOITATION OF HOSTRESPONSETypically, a parasite is viewed as challenginga host by its presence, then developing some kindof morphological or physiological adaptation toevade the host's response and thus avoid immunerejection. Citing the example of H. nodulosa,Hayunga (1989) inferred instead a more op-JFIGURE 3. Diagram showing variation in tegumentalmicrotriches of Hunterella nodulosa. A. Cross sectionof electron-dense spine. B. Cross section of microthrixshaft. C. Cross section of shaft of a spinelessmicrothrix. D. High magnification view of a rod-shapedbody found in the tegumental cytoplasm. E. Typicalcestode microthrix from the scolex. F. Branching microthrixwith short spine. G. Spineless microthrix fromposterior. H. Branching microthrix. I. Budding microthrix.J. Typical and spineless microtriches from atransitional zone of the tegument. K. Area of degeneratingmicrotriches on posterior part of worm. (FromHayunga and Mackiewicz [1975], courtesy of PergamonPress.)portunistic role for the parasite. Although theactual mechanisms of nodule formation are notknown, he suggested that the adhesive secretionof the frontal glands might also be an irritant andthat this secretion, together with the normallystrong muscular contractions of the worm, woulderode the epithelium and elicit a granulomatousresponse in the host. However, because of theworm's activity, the host is unable to completegranuloma formation. A partial granuloma isformed affording the parasite with a means ofattachment, a sheltered habitat, and ready accessto nutrients found in the intestinal lumen (Hayunga,1977, 1979b).Such a possibility suggests that the parasite isK

HAYUNGA-MORPHOLOGICAL ADAPTATIONS OF INTESTINAL HELMINTHS 871capable of far more than passive evasion of hostdefenses and that, conceivably, parasites mayevolve strategies that actively exploit the host'sresponse for their own benefit (Hayunga, 1989).Careful examination of other parasites may revealthat strategies of exploitation are far morecommon than have previously been thought(Damian, 1987).COST OF SPECIALIZATIONSpecialization in terms of morphological adaptationhas resulted in highly efficient means ofattachment for some intestinal helminths thatpresumably have given these species a competitiveedge. By adapting so well to their preferredsites, cestodes appear to be specialists with regardto space. To a somewhat lesser degree, trematodesand acanthocephalans also may be regardedas specialists. Nematodes seem less limitedin site selection by their anatomy and thus appearto be generalists in this regard, although theirhabitat selection may be restricted by physiologicalfactors. For nematodes it would appear thatniche stratification is more a question of whatthey eat rather than where they eat.Although the specialist may be highly efficient,the cost of specialization is dependence on onetype of host, as clearly demonstrated by studiesof host specificity. One need only ask the question,"Whatever happened to the parasites of thedinosaurs?" to envision the risks of a strategy ofspecialization. But, if anything, helminths haveshown themselves to be highly resilient and innovative,as shown by the ability of polystomatidmonogeneans to inhabit both the gills of tadpolesand the urinary bladders of adult frogs, or by thestrategy of neotenic development when a desiredhost is no longer available. The morphologicaladaptations described here represent only oneexample of many highly effective strategies forsurvival.ACKNOWLEDGMENTSI am grateful to Robin M. Overstreet and JohnC. Holmes, both for inviting me to speak at thissymposium and for keeping me on the programdespite the turmoil of world events this year. Iparticularly acknowledge the influence of JohnMackiewicz, who introduced me to the field ofparasitology and to the fascinating Caryophyllidea.Many of the ideas that I discussed werelearned in his classes, and the original researchthat I described was done in his laboratory. Thespecimen shown in Figure 1 was prepared by Dr.Mackiewicz. Observations on competition andsite selection by caryophyllideans were made incollaboration with Anthony J. Grey, a fellowgraduate student, now at the New York StateDepartment of Health in Albany. Finally, I givecredit to the pioneering efforts of prominent parasitologistswhom I have quoted extensively inthis paper.LITERATURE CITEDACKERT, J. E., S. A. EDGAR, AND L. P. FRICK. 1939.Goblet cells and age resistance of animals to parasitism.Transactions of the American MicroscopicalSociety 58: 81-89.BEFUS, D., AND J. BIENENSTOCK. 1982. Factors involvedin symbiosis and host resistance at the mucosa-parasiteinterface. Progress in Allergy 31: 76-177.BEGUIN, F. 1966. Etude au microscope electroniquede la cuticule et de ses structures associ6es chezquelques cestodes. Essai d'histologie comparee.Zeitschrift fuir Zellforschung 72: 30-46.BERGER, J., AND D. F. METTRICK. 1971. Microtrichialpolymorphism among hymenolepid tapeworms asseen by scanning electron microscopy. Transactionsof the American Microscopical Society 90:393-403.BRATEN, T. 1968. The fine structure of the tegumentof Diphyllobothrium latum (L.)-A comparison ofthe plerocercoid and adult stages. Zeitschrift furParasitenkunde 30: 104-112.COLWELL, R. K., AND E. R. FUENTES. 1975. Experimentalstudies of the niche. Annual Review ofEcology and Systematics 6: 281-310.CROMPTON, D. W. T. 1973. The sites occupied bysome parasitic helminths in the alimentary tractof vertebrates. Biological Reviews 48: 27-83.1975. Relationships between Acanthocephalaand their hosts. Symposia of the Society forExperimental Biology 29: 467-504.DAMIAN, R. T. 1987. The exploitation of host immuneresponses by parasites. Journal of Parasitology73: 3-13.DOGIEL, V. A. 1958. Ecology of the parasites of freshwaterfishes. In Parasitology of fishes, V. A. Dogiel,G. K. Petrushka, and Y. I. Polyanski (eds.). LeningradUniversity Press. [English translation by Z.Kabata, Oliver & Boyd, Edinburgh, xi + 384 p.,1961.]ERASMUS, D. A. 1969. Studies on the host-parasiteinterface of strigeoid trematodes. V. Regional differentiationof the adhesive organ of Apatemongracilis minor Yamaguti, 1933. Parasitology 59:245-256.1977. The host-parasite interface of trematodes.Advances in Parasitology 15: 202-242., AND C. OHMAN. 1963. The structure andfunction of the adhesive organ in strigeid trematodes.Annals of the New York Academy of Sciences113: 7-35.GREY, A. J., AND E. G. HAYUNGA. 1980. Evidencefor alternative site selection by Glaridacris laruei(Cestoidea: Caryophyllidea) as a result of inter-

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