DESCRIPTION OF ANCYLOSTOMA PLURIDENTATUM, AHOOIvWORM OF CARNIVORES, AND A REVIEW OFTHE GENUS ANCYLOSTOMA
By Benjamin SchwaetzOf the Zoological Division, Bureau of Animal Industry, Umted States De-partment of Agriculture
INTRODUCTIONAncylostoina fluridentatum was described by Alessandrini (1905)under the name UneinaHa. 'pluridentatvmh from the intestine of Felismitis, in Brazil. The special characteristics of this worm, as notedby that writer, are the two unequal pairs of teeth in the anteriorand ventral portion of the mouth capsule, the inner or median pairbeing described as very small?in fact, almost rudimentary?and thepresence of three small projections or teeth on each side of the dorsaledge of the mouth capsule. Alessandrini also noted in this species asmall process with a rugged surface on each side of the cloacal aper-ture in the male.Ancylostoma pluridentatum was not reported again for 17 years,and then Vevers (1922) reported it from the intestine of Felis tigris,in the Malay States, noting certain minor differences between hisspecimens and Alessanclrini's description of this species. Two yearslater Chapin (1924) recorded it from a South American carnivore{Felis tigrina), which had died in the National Zoological Park inWashington, D. C. Chapin merely noted the presence of this speciesin the United States, but did not discuss the morphology of theworm.In the opinion of Lane (1918) this species should be made thetype of a new genus. ? Lane has also considered the possibility thatAlessandrini may have misinterpreted the structures on the dorsaledge of the mouth capsule as well as the two rugged structures nearthe cloacal aperture of the male, in which case the question of thepossible identity of Ancylostoma pluridentatwin with AncyclostomaNo. 2697,?Proceedings U. S. National Museum, Vol. 72, Art, I55216?27 1 . 1
2 PROCEEDINGS OF THE NATIOI^AL MUSEUM vol. 72hraBiliense deserved serious consideration. Lane concluded, how-ever, that : " The doubt can only be cleared up by the reexaminationof Alessandrini's original material, if this be still in existence."Darling (1923) appears to accept the view that A. pluridentatwnis probably identical with A. hrasiliense, basing this view on Ales-sandrini's statement that the inner pair of teeth is almost rudi-mentary, a feature noted by Darling as well as by other investigatorswith reference to the corresponding teeth of A. hrasiliense. Darlingstates further that there is a possibility that the three dorsal teethon each side of the mouth capsule as noted by Alessandrini may havebeen the result of some pathological condition.In view of the doubt expressed by Lane and Darling concerningthe present status of Ancylostoma pluridentatuin the writer exam-ined the specimens collected by Chapin from Felis tigHna as wellas specimens of this species from two other lots present in theHelminthological collections of the United States National Museum.One lot was collected about a year ago from the intestine of aSouth American carnivore {Felis eyra) that had died in the IsTa-tional Zoological Park, the specimens having been determined byChapin and the writer. The second lot was discovered by thewriter in the course of examinations of various specimens ofhookworms from carnivores present in the helminthological col-lections of the United States National Museum. The lot in ques-tion was collected in January, 1905, from Felis species by Dr.Albert Hassall in the course of a post-mortem examination of theanimal which had died in the National Zoological Park. Thesespecimens were later examined by Dr. C. W. Stiles, of the hygieniclaboratory of the United States Public Health Service, who labeledthem ''''Ancylostorma^ new species." It should be noted in this con-nection that Doctor Stiles's determination was made before Ales-sandrini's description of A. fluridentoAum was published.The observations recorded in this paper not only confirm thespecific validity of A. fluridentatvmh^ based on a study of specimensfrom the type locality, but also clear up certain points in themorphology of these worms that led Darling to the view thatAncylostovia 'pluridenta^jmh and Ancylostom.a hraziliense are prob-ably identical.DESCRIPTION OF ANOYLOSTOMA PLURIDBNTATUMThe features of the mouth capsule that differentiate AncylostoTiiapluridentatuTTh from all other species of the genus Ancylostoma arethe structure of the two pairs of teeth in the anterior and ventralportion of the mouth capsule, coupled with the presence of threesmall teeth on each side of the dorsal wall of the mouth. (Fig. 1.)As has already been said these features were noted and emphasized by
ART. 1 Al\ CYLOSTOMA PLURIDENTATUM SCHWARTZ 3Alessandrini who described the inner ventral teeth as being verysmall in comparison with the large outer teeth. So far as concernsthe relative size of the pair of inner teeth, the writer has notbeen able to confirm Alessandrini's findings, as the inner pair ofteeth in the specimens examined was found to be of good size. How-ever, Alessandrini's interpretation of the size of the inner teeth mayhave been due to his study of imperfectly cleared specimens or to aninterpretation of the tips of the teeth as teeth with the remainingbroad portion regarded as a basal plate to which they were attached,instead of regarding the entire structure as a tooth in each case asthe writer has regarded them. In specimens imperfectly cleared onlythe tips of the inner teeth which point caudad are visible, since theyprotrude beyond the margin of the outer teeth, the remaining portionof these teeth, which lie in a more or less horizontal plane, beingcovered by the outer teeth. When the buccal capsule is viewedthrough the ventral surface, however, the inner teeth which are moreventrally placed than the outer teeth, stand out quite distinctly inwell cleared specimens, and are seen to be discrete structures, and ofgood size. The tips of the outer teeth are relatively large and con-spicuous, and have the shape of a triangle.In certain specimens from Felis tigrina the tips of the outer teethwere found to be truncated in a number of specimens (fig. 4), resem-bling in this respect the corresponding teeth of Ancylosioina hrazili-ense^ in which similar malformations of the outer teeth are by nomeans uncommon. In A. 'pluridentatmn the abnormality in the outerteeth is sometimes unilateral and sometimes bilateral. In some speci-mens the tip of the tooth appears to be cut off cleanly whereas inother specimens it presents the appearance of an uneven surface sug-gestive of erosion. Abnormalities were also observed in the threepairs of small dorsal teeth in specimens from Felis tigrina. The mid-dle tooth on one or both sides is the one affected, and appears to beeroded in certain specimens. In some specimens the tips of the teethare almost entirely absent, the characteristically pointed tooth beingreplaced by a slightly concave or by a more or less irregularly flat-tened cuticular elevation. Normally the dorsal teeth end in sharppoints. No abnormalities of the teeth were observed in specimensfrom Felis eyra and from Felis species.The cephalic papillae are very conspicuous and are located anteriorto the nerve ring. Their position with respect to the middle of theesophagus is by no means constant, being either slightly anterior orposterior to the middle of the esophagus. The position of the excre-tory pore is slightly posterior to the nerve ring.Male.?The males are from 7 to 8 mm. long by about 294;u, wide inthe middlo of the body. The maximum width of the body is imme-diately in front of the bursa which has a diameter of from 302 to
4 PEOCEBDINGS OP THE ]SrATI01?J"AL MUSEUM vol.72310/^. The buccal capsule is from 131 to 178/* wide. The esophagus(fig. 3) is from 638 to 740/* long by 168/x in maximum width. Thenerve ring is located anterior to the middle of the esophagus, dividingthe latter into two parts having an approximate ratio of 4 to 6. Ina specimen from Felis tigrma the cervical papillae divide the esoph-agus into two parts, the ratio of the anterior part to the posteriorpart being 17 to 13, whereas in a specimen from Felis eyra this ratiois 25 to 17.The spicules are long and slender (fig. 6), and are from 1.15 to1.17 mm. long. The short gubernaculum is from 60 to 74/i long bylOjU. wide. The bursa (fig. 5) is from 470 to 554/x wide when spreadout. The ventro-ventral ray is a little longer and also somewhat widerthan the latero-ventrai ray. The tips of these rays extend to withina short distance from the margin of the bursa. The externo-lateralray, which terminates at a considerable distance from the edge ofthe bursa, is much smaller than the medio-lateral and postero-lateralrays from which it diverges. The medio-lateral and postero-lateralrays are large and parallel, their tips extending almost to the poste-rior margin of the lateral lobes of the bursa. The distance betweenthe tips of the externo-lateral rays when the bursa is viewed fromthe dorsal aspect is 180/x. The dorsal ray is from 151 to 168/a longand divides into two branches at a distance of about 35/(, from theposterior end. Each branch of the dorsal ray is tridigitate. Theprebursal papillae are located at a distance of 504,a, from the posteriormargin of the lateral lobes of the bursa. As noted by Alessandrini,a rugged structure is present on each side near the anogenital opening(fig. 6), the surface of which appears granular in optical section.Female.?The females are from 10 to 11 mm. long by 344 to 378/awide in the region of the vulva. The maximum diameter of thebuccal capsule varies from 168 to 210ft. The esophagus is from 739to 806/1 long by 185 to 210/a in maximum width. The cephalicpapillae divide the esophagus into two unequal parts, the ratio of theportion anterior to the papillae to that posterior to the papillae being26 : 20 in a specimen from Felis tigrina., whereas in a specimen fromFeUs eyra the ratio is 22 : 23. The nerve ring is anterior to thecephalic papillae, the excretory pore being in a position inter-mediate between the nerve ring and cephalic papillae.The vulva is located near the beginning of the posterior third ofthe body. In an immature specimen about 8 mm. long the vulva islocated at a distance of 2.8 mm. from the tip of the tail. In a speci-men about 11 mm. long the distance from the vulva to the tip of thetail is 3.3 mm. The tail (fig. 2) is from 126 to 176/t long and isgradually attenuated. The slender bristle that is inserted in the tipof the tail is from 17 to 25/1 long.
AST. 1 AN-CYLOSTOMA PLUEIDENTATUM SCHWAETZ
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/OO/J.
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loojm
Figs. 1-6.
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Ancylostoma pluridentatum alessandrini, 1905. 1, Buccal capsule ; 2,POSTBKIOE end OF FEMALE ; 3, ANTERIOR PORTION OF WORM ; 4, PAIR OF VENTRAL TEETH ;5, BURSA OF MALE (SOMEWHAT DIAGRAMMATIC) ; 6, REGION OF CLOACAL OPENING SHOWINGSPICULES. a., ANUS ; C. p., CERVICAL PAPILLAE ; d., DORSAL RAT ; 6. d., EXTERNO-DORSALRAT ; e. I., EXTERNO-LATERAL RAY ; int., INTESTINE ; }. V., LATERO-VENTKAL RAY ; m. I.,MEDIO-LATERAL RAY ; n. r., NERVE RING ; p. I., POSTERO-LATERAL RAY ; V. V., VENTRO-VENTRAL RAY55216?27?2
6 PEOCEEDINGS OF THE NATIONAL MUSEUM vol.72DISCUSSIONIt will be noted from the description that there are certain slightdifferences in the morphology of the worms from Felis tigrina andFelis eyra, the most important differences being in the position of thecephalic papillae and in what appear to be malformations of theteeth. In specimens from Felis tigrina the cephalic papillae arelocated anterior to the middle of the esophagus and but slightlyposterior to the nerve ring, whereas in specimens from Felis eyrathe cephalic papillae are located posterior to the middle of theesophagus and considerably posterior to the nerve ring. Otherminor differences in specimens from the two hosts were noted butthese were rather variable, and possibly due to the fact that theworms from F. tigrina are not fully grown.So far as concerns Lane's suggestion that Ancylostoma flwriden-tatum represents a new genus, the writer is of the opinionthat Lane's judgment was sound in not actually proposing a newgeneric name, that the special differentiating characters of this wormshould be regarded at this time as of specific rank, and that for thepresent, at least, these parasites may be left in the genus Ancylostomasince they possess all of the essential characters of this genus. Iffor no other reason than that of convenience, the creation of a newgenus for A. plv/ridentatum is avoided in this paper as notjustified at the present time owing to the comparatively small numberof easily differentiated species now assigned to the genus Ancylos-toma. In general we feel that dividing a comparatively small andcoherent genus to form from one of its species a new genus containingonly that species frequently adds unwarrantably to the already bur-densome nomenclature with which the taxonomist must cope. Shouldother forms be found to share with A. pluridentatum characters notshared by other species assignable to Ancylostom^a, it will then betime to consider the proposal of a genus for this group,SPECIES OF THE GENUS ANCYLOSTOMAYorke and Maplestone (1926) list the following species as belong-ing to the genus Ancylostoma: A. duodenale (Dubini, 1843) Crep-lin, 1845, type species of the genus; A. braziliense de Faria, 1910;A. caninum (Ercolani, 1859) ; A. conefati (Solanet, 1911) ; A. gil-soni Gedoelst, 1917; A. malayanum (Alessandrini, 1905); A. mdni-TYium (Linstow, 1906) ; A. mucronatum (Molin, 1861) ; A. mycetes^new name, Yorke and Maplestone, 1926 { = DiploodonquadTidentatuonMolin, 1861); A. pluridentatum (Alessandrini, 1905). Molin's twospecies are inadequately described, but his figures indicate quiteclearly that they belong to the genus Ancylostoma. His figure ofA. mucronatum shows two equal spicules nearly one-fourth as longas the total length of the male. In this connection it is interesting
AET. 1 ANCYLOSTOMA PLURIDENTATUM SCHWAETZ 7to note that the males of A. conepati, which have an average lengthof 8.8 mm., have long spicules, their average size being 2 mm., theratio of the length of the spicules to the total length of the bodybeing practically the same in this species as in A. wucronatum. Thefact that both of these species occur in South America is of furtherinterest in connection with their possible identity. It may be noted,however, that A. onucronatum is from an edentate, Dasypus gilvipes^whereas A. conepati is from a carnivore, Conepatus suffocans.However, owing to the paucity of morphological data regardingA. mua'onatuQn the question of the possible identity of this formwith A. conepati is left open. Both of these sjDecies appear to beclosely related to A. caninutn^ differing from the latter primarily inthe lengths of the spicules. Molin's figure of Diploodon quadriden-tatum {=A mn/cetis) shows two pairs of well-developed teeth in theanterior portion of the mouth capsule. Male specimens of thisspecies were not available to Molin, his description and figure beingbased on a female. Whether this form, collected from a primate{Mycetes coraya), is A. duodenale or whether it represents a dis-tinct species can not be decided on the basis of Molin's description.A. mini'muni is inadequately described, there being no reference toteeth in the anterior portion of the buccal capsule. Von Linstow'sfigure of the bursa suggests that the species may belong to the genusAncylostoma^ although the possibility that he was dealing with aspecies of Uncinaria must also be taken into consideration. So faras can be judged from the arrangement of the bursal rays, thisspecies is related to forms such as A. hraziliense and other speciesof this genus, which have but two pairs of teeth in the anterior por-tion of the buccal capsule. A. gilsoni Gedoelst, 1917, from Sciurusprevosti^ is regarded by the writer as a synonym of A. hra-ziliense, since the figures and measurements of this species givenby Gedoelst agree in practically all respects with available figuresand descriptions of A. hrazilieiise and with the writer's ob-servations on that species based on a study of specimens from theUnited States, South America, and various parts of Asia. Gedoelsthas apparently created A. gilsoni largely on the basis of host rela-tionship and does not point out in what respects this species differsfrom A. hraziliense. Our present knowledge of host relationshipsof species of the genus Ancylostoma does not appear to justify theerection of a new species on this basis alone, since certain species ofthis genus are known to occur in aberrant hosts. This is especiallytrue with reference to A. hraziliense, which occurs not only in speciesof carnivores but also occasionally in man, in which host it attainsfertile maturity.Lane (1916) has called attention to the fact that in species of thegenus Ancylostoma which contain three pairs of teeth in the anterior
8 PROCEEDINGS OF THE NATIONAL MUSEUM vol.72
ventral portion of the mouth capsule, the medio-lateral and postero-lateral rays are divergent, the cleft between these rays being deepertlian that between the externo-lateral and medio-lateral rays, whereasin forms having two pairs of teeth in the anterior ventral portion ofthe buccal capsule the medio-lateral and postero-lateral rays lie closetogether and parallel, the cleft formed between these rays not beingdeeper than that formed between the externo-lateral and medio-lateral rays.The following key will serve to differentiate the species of Ancy-lostoma'^ and to indicate their relationships.
I. Three pairs of teeth in anterior ventral portion of buccal capsule; medio-lateral and postero-lateral rays divergent.1. Inner pair of teeth small or rudimentary A. duodenale.2. Inner pair of teeth well developed.A. Species inadequately described; from an edentate {Dasypusgilvipes) A. miicronatum.B. Species adequately described ; from carnivores.a. Spicules 600^900 fi long A. caninum,1). Spicules l.S-22 mm. long A. conepati.II. Two pairs of teeth in anterior ventral portion of buccal capsule ; medio-lateral and postero-lateral rays close together and parallel.1. Inner pair of teeth small or rudimentary.A. Three pairs of small toothlike projections present on dorsal wallof buccal capsule A. pluridentatum.5. Toothlike projections not present on dorsal wall of buccalcapsule A. braziliense.2. Inner pair of teeth well developed.A. Species inadequately described; from a primate {Mycetescoraya) A. mycetis,B. Species adequately described; from carnivores (Ursidae).A. malayauuiu.In connection with the above key it is worth noting that the teethin the anterior ventral portion of the buccal capsule of species ofAnoylostoTrm show a series of stages which may be interpreted asbeing either progressive or regressive in nature. In A, caninum^ A.conepati, and A. mucronatum three pairs of well-developed teethare present in the anterior ventral portion of the buccal capsule; inA. duodenale the inner of the three pairs of teeth is very small, infact, almost rudimentary; in A. malofyan'mrh and, so far as can bejudged from Molin's figure, in A. tmjceth, only tAvo pairs of well-developed teeth are present in the anterior ventral portion of thebuccal capsule; in A. 'pluridentatum and in A. ira^iliense two pairs ofteeth are present, the inner pair of teeth being reduced in size, the
1 A. minimum is not included in this key owing to the ahsence of knowledge regardingthe presence of teeth in the anterior ventral portion of the buccal capsule. Assumingthat von Linstow's species belongs to the genus Ancylostoma, it has affinities with theforms in Group II so far as can be judged from his figure of the bursa.
ART. 1 ANCYLOSTOMA PLURIDEN^TATUM SCHWARTZ 9buccal capsule containing in the anterior ventral portion one pair ofwell-developed teeth and one pair of small or rudimentary teeth. Incertain specimens of A. 'braziliense collected by the writer from a catwhich was shipped from Florida the inner pair of small teeth wasfound to be entirely absent, whereas in other specimens from the samehost it was present. This observation suggests the possibility of theoccurrence of a variety of Ancylostoma 'braziliense containing but asingle pair of teeth. Such variation, if germinal in character and notdue merely to external causes, undoubtedly represents an incipientspecies. It is suggested, purely as an interesting speculation, that thevarious species of Ancylostoma containing less than three pairs ofwell-developed teeth in the anterior oral margin may have arisenfrom forms containing three pairs of teeth, each species representinga mutation. REFERENCESAxesSANDRiNi, Gitjlio.1905.?Su di alcune uncinariae parassite deH'uomo e di altri vertebrati,Boll. Soc. zool. ital., Roma, vol. 14, pp. 23-48, pis. 1-i.Chapin, E. a.1925.
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\_AnGylostoma, pluridentatum (Aless.) from Felis Ug^-ina-l [Readbefore Helm. Soc. Wash., Oct. 17], Journ. Parasitol., Urbana, 111., vol.12, p. 113.Darling, Samuel T.1924. Ancylostomot 'braziliense de Faria, 1910, and its occurrence inman and animals, Amer. Journ. Hyg., Bait., vol. 4, pp. 416-448, figs. 1-10.Gedoelst, L.1917.?Nematodes parasites du Sciurus prevosti de Sumatra, Rev. zool.Africaine, Brux., vol. 5, pp. 153-162, figs. 1-3 ; footnote by H. Schoute-den, p. 153 [MS dated mai].Lane, Clayton.1916.?The genus Atwylostoma in India and Ceylon, Indian Journ. Med.Research, Calcutta, vol. 4, pp. 74^92, pis. 1-3.VON LinSTOW, O.1906.?Helminthes from the collection of the Colombo Museum, SpoliaZeylanica, Colombo, pt. 11, vol. 3, pp. 163-188, pis. 1-3, figs. 1-55.McLiN, Raffaele.1861.?II sottordine degli acrofalli ordinate scientificamente secondo irisultamenti delle indagini anatomiche ed embriogeniche [Presented 14gennajo], Mem. r. 1st. Veneto di sc, lett. ed arti, Venezia (1860), vol.9, pp. 427-633, pis. 25-33.YBVEais, G. M.1923.?On the parasitic nematoda collected from mammalian hosts whichdied in the Gardens of the Zoological Society of London during theyears 191&-1921 ; with a description of three new genera and three newspecies [Read Nov. 7, 1922], Proc. Zool. Soc. Lond., 1922, pt. 4, pp.901-919, figs. 1-10.YoEKE, Waerington, and Maplestone, P. A.1926.?The nematode parasites of vertebrates. With a foreword byC. W. Stiles, xi+536 pp., 307 figs. London.o