Superfamily H E T E R A K 0 1 D E A Chabaud, 1957. Ascaridina : three distinct lips, dorsal with two double papillse, ventral with a double ventral papilla each ...
A R E V I E W OF T H E NEMATODE S U P E R F A M I L Y HETERAKOIDEA. B y WILLIAM G. INGLIS, Department of Zoology, British Museum (Natural History). IN outlining a new classification of the nematode suborder Ascaridata, Chabaud (1957) based his arrangement of the superfamily Heterakoidea mainly on the classification proposed by Freitas (1956) for the family Heterakidae. Freitas based his suggestions almost wholly on the information available in the literature, which is in many cases misleading. Chabaud's proposals are otherwise reasonable and since he intends to base further publications on this classification it appears necessary to present m y own conclusions on the groupings which can be recognized within the superfamily. These have been reached after an extensive study, which is still continuing, of a large number of specimens ; a study which is being carried out to revise the family Heterakidae as fully as possible. This revision will not be completed for some time but the major groupings which are proposed here appear to be settled and it is unlikely that the work which remains to be done will upset them to any extent. The names listed under each genus, however, in most cases only represent nominal species which possess the combination of characters diagnostic of each genus and it is not suggested, particularly in the genus Strongyluris, that they are all valid. It is not intended to give here the detailed reasoning behind most of the groupings, much of which is clear from the groupings themselves. However something must be said in support of the division of the superfamily into two families and the exclusion from it of the family Ascaridiidae. The latter family is discussed elsewhere (in press, J. Helminth) and has always tended to be rather problematical in its relationships. Chabaud considers it a heterakoid but I prefer to consider it, at ledst provisionally, a member of the Ascaridoidea. The superfamily Heterakoidea, as constituted here, is a fairly homogeneous morphological group within which are two distinct sub-groups, here considered families--Heterakidae and Aspidoderidae. That they are related there can be little doubt b u t to treat them as subfamilies, as is done b y Chabaud, masks the extreme specialization which is shown b y the aspidoderid group, a specialization culminating in Lauroia in which the structure of the head is highly modified and the structure of the tail is simple. I have been able to study some of the syntype series of Lauroia travasossi (the type species of the genus), through the courtesy of Dr. J. F. Teixeira de Freitas, and the head has the interconnecting lobes to the lips which are characteristic of the aspidoderids and may be considered to represent a highly specialized form of the head characteristic of the genus Paras2~idodera (see Inglis, 1957). While it is recognized
906
W. G. Inglis on the superfamily I-Ieterakoidea
that the heterakids and aspidoderids have most probably been derived from a similar ancestral form, I consider the latter group to represent the radiation of an isolated group which has diverged to such an extent that it should be recognised as a distinct family. Further Chabaud's classification into three subfamilies Lauroiinae, Aspidoderinae and Heterakinae does not sufficiently represent the similarities between the aspidoderids and Lauroia, and in addition does not allow the morphological trends within the heterakids to be fully demonstrated. The subfamily Schneidernematinae Freitas, 1956 was accepted by Chabaud b u t its inclusion within a separate subfamily can only be justified b y our lack of knowledge of its true relationships and I do not consider it to be a heterakid, and it is considered elsewhere (in press, J. Helminth), preferable to include it in the family Asearidiidae. Superfamily H E T E R A K 0 1 D E A Chabaud, 1957. Ascaridina : three distinct lips, dorsal with two double papillse, ventral with a double ventral papilla each and a single papilla each laterally, external to the amphid ; lining of mouth cavity divided into three distinct parts, one corresponding to each lip (anterior cuticular flanges) ; pharyngeal, portions embedded in mass of lips : oesophagus with posterior bulb, tri-valvulated and with no obvious isthmus ; no intestinal or oesophageal appendices: Male: circular pre-cloacal sucker with definite, simple cuticular r i m ; two spicules. F e m a l e : eggs not embryonate in utero, thick-shelled. Family Heterakidae Railliet & Henry, 1914. Heterakoidea : lips rounded, not connected b y lateral lobes ; cordons, when present, not anastomosing and poorly developed; oesophagus fairly short and stout. Males : caudal alae generally present ; number of caudal papillm small ; spicules m a y be unequal and dissimilar; gubernaculum generally reduced or absent ; tail generally relatively short. Subfamily HE~R~KXz¢~ Railliet & Henry, 1912. Heterakidae : lips not off-set from the body ; anterior cuticular flange of lips generally not projecting anteriorly ; interlabia, or their homologues, present. Male: pre-cloaeal sucker relatively large; caudal alae well developed, supported b y long, thin papillm ; gubernaculum lacking; spicules frequently dissimilar ; no papillae on general body surface. Type genus : Heterakis Dujardin, 1845. Hosts and geographical distribution : mainly birds, a few species of uncertain systematic position in mammals. Cosmopolitan. Genus I'IETERAKIS Dujardin, 1845. Heterakinae : lips without obvious inter-labia, but with slight elevations between them which m a y be homologous with interlabia ; no interlabial grooves or cordons. Type species : H. gallinarum (Schrank, 1785), Madsen, 1949.
W. G. Inglis on the superfamily Heterakoidea
907
Hosts and geographical distribution: mainly galliform birds. Cosmopolitan. Other species : The following species can be distinguished with certainty: H. alata Schneider, 1866; H. bancrofti Johnston, 1912; H. beramporia Lane, 1914 ; H. bosia Lane, 1914 ; H. brevispiculum Gendre, 1911 ; H. dispar (Sehrank, 1790), Dujardin, 1845 ; H. isolonche Linstow, 1906 ; H. ]curilensis Oschmarin, 1949; H. macrospiculum Ortlepp, 1939; H. nattereri Travassos, 1923 ; H. parva Maplestone, 1931 ; H. psophiae Travassos, 1913 ; H. spalacis Marcu, 1930 ; H. spumosa, Schneider, 1866. It is probable that H. indica Maplestone, 1932--which may be only an abberent gallinarum--should be included in the previous list with H. lingnanensis Li, 1933 and H. yamadori Yamaguti, 1941 as synonyms. The following nominal species appear to be indistinguishable from species in the previous list. H. altaica Spaul, 1929 (?) from H. dispar ; H. bonasae Cram, 1927-(?) H. isolonche ; H. brasiliana Linstow, 1899--(?) H. alata ; H. caudata Linstow, 1906--H. dispar ; H. caudebrevis Popowa--H. gallinarum ; H. dahomensis Gendre, 1911---H. spumosa; H. hastata Chandler, 1926--H. isolonche ; H. hyperborea Swinyard, 1931--H. dispar ; H. lanei Chandler, 1926--H. isolonche ; H. neoplastica Wassink, 1917--H. isolonche ; H. papillosa (Bloch, 1782), Cram, 1927~-H. dispar ; H. parisi Blanc, 1913-H. gallinarum ; H. pedeocetis Mawson, 1956--(?) H. gallinarum ; H. putaustralis Lane, 1914--H. isolonche ; H. stylosa Linstow, 1907--H. dispar ; H. tenuicauda Linstow, 1883--(?) H. dispar ; H. tragopanis Lal, 1942---H. isolonche ; H. variabilis Chandler, 1926--(?) H. parva ; H. vesicularis (Froelich, 1791)--H. gallinarum. It is, at present, impossible to determine to what species the following names are referable on the basis of the descriptions available and in most cases it is impossible t o trace their type specimens. They are therefore listed as species inquirendae. Strongyluris acuticaudata Cobbold, 1861 (it might be better to treat this name as a nomen dubium) ; H. chenonettae Johnston, 1912 ; H. flexuosa Schneider, 1866 ; H. gracilis Linstow, 1883 (unlikely this is a Heterakis in the modern sense) ; H. longecaudata Linstow, 1879 ; H. pucilla Linstow, 1906 ; Strongyluris spiculatus Cobbold, 1861 (probably better to consider this a nomen dubium) ; Ascaris valdemucronata Molin, 1860 (unlikely to be Hetera]cis in modern sense). H. pavonis Maplestone, 1932 is almost certainly a synonym of Pseudaspidodera pavonis. Genus ODO•TOTERAKXS Skrjabin & Schikhobalova, 1947. Heterakinae : inter-labia modified as inter-labial grooves which are non-recurrent. Type species : O. crypturi (Baylis, 1944), Skrjabin and Schikhobalova, 1947. Host and geographical distribution : mainly tinamous, South America
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W. G. Inglis on the superfamily tteterakoidea
(except O. interlabiata, from Rhizothera longirostris, London Zoological Gardens). Other species : O. fariai (Travassos, 1914) comb. nov. ; O. multidentata (Bay]is, 1944), Skrjabin and Schikhobalova, 1947; O. interlabiata (Ortlepp,1923), comb. nov. ; O. valvata (Schneider, 1866) comb. nov. The Heteralcis arquata of Travassos, 1913 is indistinguishable from O. crypturi while H. slcrjabini Cram, 1927 (H. arquata of Skrjabin, 1916) is indistinguishable from H. arquata Schneider, 1866, which in its turn is indistinguishable from H. alata Schneider, 1866. Genus ~)SEUDASPIDODERA Baylis & Daubney, 1922. Heterakinae : inter-labia modified as cordons, divergent, recurring and not anastomosing. Males : spicules dissimilar. Type species : P. pavonis Baylis & Daubney, 1922. Host and geographical distribution: Phasianidae, India and related areas. Other species : P. jnanendrae Chakravarty, 1938 (this species was described as having anastomosing cordons but this appears to be an artefact, probably due to fixation); P. voluptuosa Chandler, 1926; P. spinosa Maplestone, 1932 (this species which is described as possessing cordons which anastomose and are lined by spines m a y warrant generic separation when more material is collected).
Subfamily MET~ER~KIlC~E, nov. Heterakidae : lips not off-set from b o d y ; no inter-labia; excretory pore opens into a large vesicle ; Male : pre-cloacal sucker relatively small ; caudal alae fairly prominent, supported by three, exceptionally by four, large fleshy papillm ; large number of small sessile papillae on tail ; Female : vulva covered by flap developed from the anterior lip of opening ; common uterine trunk runs posteriorly. Type genus : Meteteralcis Karve, 1930. Host and geographical distribution : reptiles, amphibia and mammals (Hystrix). Oriental region in the widest sense (India, Ceylon, China, Japan, East Indies, Burma). Genus METETERAKIS Karve, 1930. Meteterakinae : no cordons; body generally bearing small papillae over entire surface. Males: spicules equal and identical; indefinite gubernaeular mass developed from walls of cloaca, except possibly in M. triaculeatus ; posterior lip of cloacal opening covered by small cuticular granulations. Type species : M. govindi Karve, 1930. Hosts and geographical distribution: reptiles and amphibia, distributed as for the subfamily. Other species : M. cophotis (Bay]is, 1935) comb. nov. ; M. japonica (Wilkie, 1930) comb. nov. ; M. longispiculata (Bay]is, 1929) comb. nov. ; M. mabuyi
W. G. Inglis on the superfamily Heterakoidea
909
(Chakravarty, 1944) comb. nov. ; M. singaporensis (Sandosham, 1954) comb. nov. ; M. triaculeatus (Kreis, 1933) comb. nov. The following nominal species appear to be indistinguishable from species in the previous list : Spinicauda bufonis Yamaguti, 1935 from M. govindi ; Africana howardi Li, 1933--M. japonica ; A. varani Maplestone, 1931--(?) M. govindi. Genus GIR]~TERAKIS Lane, 1917. Meteterakinae : straight cordons, one arising from each inter-labial space ; body without small papillse on surface ; Males : spicules equal, identical and very elaborate; no gubernacular mass; posterior lip of cloacal opening without cuticular granulations. Type species : Gireterakis girardi Lane, 1917. Host and geographical distribution : Hystrix spp., India. Subfamily SplNIC~I)I~Ag Travassos, 1920. tteterakidae : lips off-set from body ; no inter-labia or cordons ; lateral fields prominent. Male: spicules equal, identical and simple; papillse do not generally support caudal alae, when alae present ; if t h e y do support alae the tail is short and pre-cloacal sucker is directed posteriorly. Type genus : Spinicauda Travassos, 1920. Host and geographical distribution : reptiles and amphibia. Cosmopolitan. Genus SPI~ICAVDA Travassos, 1920. Spinicaudinae : anterior euticular flange projects slightly anterior to mass of lips. Male : tail long with relatively small sessile papillm and no obvious c~udal alae; gubernaculum present; pre-cloacal sucker relatively small. Type species :S. spinicauda (l~udolphi, 1819) Trav~sos, 1920. Host and geographical distribution: cosmopolitan in reptiles and amphibia. Subgenus S P I ~ I c A v D A. Male tail long with small sessile papillae ; pre-cloacal sucker relatively small directed ventrally. Other species : S. (S.) australiensis Baylis, 1930; S. (S.) sonsinoi (Linstow, 1894) Travassos, 1920; S. (?) mathevossianae Skarbilovich, 1950 (it is not certain from the description of this species whether it is a Spinicauda or Meteteralcis ). S. campanula (Linstow, 1899), Travassos, 1920 is indistinguishable from S. (S.) spinicauda ; S. amarali Pereira, 1935 from S. (S.) spinicauda ; S. grimmae Belle, 1957 from S. (S.) sonsinoi. Subgenus M o A R c I R I A (Freitas, 1956). Male tail fairly short with relatively large papill~e ; pre-cloacal sucker directed posteriorly, relatively large.
910
W. G. Inglis on the superfamily Heterakoidea
Type species: S. (M.) alvarengai (Freitas, 1956). Host and geographical distribution: reptiles, Africa and South America. Other species : S. (M.) icosiensis (Seurat, 1917), Travassos, 1920. Aplectana pharyngeodentata Belle, 1957, of which I have seen paratypes, is indistinguishable from S. (M.) icosiensis. Genus AFRICANA Travassos, 1920. Spinicaudinae : anterior cuticular flange of lips not projecting anterior to main mass ; lateral alae present. Males : pre-cloacal sucker small ; spicules equal and identical, alate ; gubernacular mass present; small sessile papillae on tail which do not support the fairly well developed caudal alae ; caudal alae stop anterior to the cloacal opening. Type species : A. africana (Gendre, 1909) Travassos, 1920. Host and geographical distribution : reptiles and amphibia. Africa. Heterakis acuticeps Gedoelst, 1916, H. brodeni Gedoelst, 1916 and Africana astylosterni Sandground, 1933 are indistinguishable from the type species. Genus ST~O~GYLURIS Muetler, 1894. Spinicaudinae : anterior cuticular flange of lips very large ; cuticle of body generally bearing small sessile papillae. Male : posterior end trunc a t e ; pre-cloacal sucker prominent, directed posteriorly; caudal alae well developed supported by short, very stout papillae ; spicules equal and non-alate ; no gubernaculum. Type species : S. brevicaudata Mueller, 1894. Host and geographical distribution : reptiles and amphibia, cosmopolitan. Other species : S. acaudata Caballero, 1941; S. bengalensis Chakravarty, 1936; S. bufonis ¥ a m a g u t i & Mitunaga, 1943; S. calotis Bay]is & Daubney, 1923; S. chamaeleonis Baylis & Daubney, 1922; S. davisi Harwood, 1948 ; S. elegans (Gendre, 1904) Railliet & Henry, 1914 ; S. gigas Spaul, 1923; S. gonyocephali Kreis, 1940; S. karavirensis Karve, 1938; S. media Harwood, 1935 ; S. meridionalis Kreis, 1938 ; S. ornata (Linstow, 1897) Railliet & Henry, 1914; S. oscari Travassos, 1923; S. paronai (Stossich, 1902) Rail]iet & Henry, 1914 ; S. ranae Reiber, Byrd & Parker, 1940 ; S. readi Rothman, 1954 ; S. riversidensis Edgerly, 1952 ; S. rubra Harwood, 1935; S. sai Travassos, 1926; S. similis Caballero, 1938 ; S. streptoesophageus Connal, 1912 ; S. tridentata Kreis, 1940. It is doubtful if more than half of the nominal species listed above can be distinguished, the position being complicated by the description of virtually every sample collected as a new species so that almost the only specimens available for study are types of one kind or another. It is, however, possible to say that S. loveridgei Spaul, 1923 is indistinguishable from S. gigas. Further the type series of S. paradoxus Sandground, 1933, a species reported from a bird, consists of three male and five female
W. G. Inglis on the superfamily Heterakoidea
911
specimens which are in m a n y ways abnormal. One specimen has five caudal papillm, the spicules appear to be lacking and the lips are not fully developed while the other two specimens have the usual ten pairs of caudal papillm. There can be little doubt that these specimens represent an accidental infection and S. paradoxus must be treated as the name of a group of partly teratological specimens. Family Aspidoderidae Freitas, 1956 (sensu Inglis, 1957). Heterakoidea : three square lips connected by lateral lobes; cuticle at anterior end of body thickened as a cephalic cap ; oesophagus long and narrow with small posterior oesophageal bulb. Males : no caudal alae ; gubernaculum present ; spicules generally massive, equal and identical ; m a n y small sessile papillm, all of approximately the same size, generally present on tail which is long and narrow. Host and geographical distribution : edentates, marsupials and hystricomorphs in South America and related areas. Subfamily ASPIDODERI~AE Skrjabin & Schikhobalova, 1947. Aspidoderidae : cephalic cordons present ; lateral lobes of lips complex. Type genus : Aspidodera Railliet & Henry, 1912. Hosts : marsupials and edentates. Genus ASPIDODERA Railliet & Henry, 1912. Aspidoderinae : cephalic cordons recurrent and anastomosing. Type species : A. scoleciformes (Diesing, 1851) Railliet & Henry, 1912. Other species : A . faciata (Schneider, 1866), Railliet & Henry, 1912; A. harwoodi Chandler, 1932 ; A . raillieti Travassos, 1913 ; A. subulata (Molin, 1860) Railliet and Henry, 1912 ; A. vazi, Proen~a, 1937. Genus A~SI~UPTOD]~RA Skrjabin & Schikhobalova, 1947. Aspidoderinae ; cephalic cordons not anastomosing. Type species : A. ansirupta (Proen~a, 1937) Skrjabin & Schikhobalova, 1947. Genus SEXANSODERA Skrjabin & Schikhobalova, 1947, Aspidoderinae : cordons recurrent and anastomosing with that on the dorsal lip forming a double loop. Type species : S. binansata (Railliet & Henry, 1913) Skrjabin & Schikhobalova, 1947. Other species : S. agoutinae (Cameron & Reesal, 1951) Freitas, 1956. Subfamily L,~vRoxIN~s Skrjabin & Schikhobalova, 1951. Aspidoderidae : cephalic cordons lacking; lateral lobes of lips not complex. Type genus : Lauroia Proen~a, 1938. H o s t s : edentates and hystricomorphs.
912
W. G. Inglis on the superfamily Heterakoidea
Genus LAURO~ Proenga, 1938. Lauroiinae : cephalic cap modified into three " plates " which are slightly undercut posteriorly. Male: posterior end relatively simple, wi~hou~ a gubernaculum, relatively few papillae and a reduced pre-cloacal sucker. Type species : L. Sravassosi Proen~a, 1938. Other species : L. dasypi Barroeta, 1956; dadensis Cameron, 1939.
L. intermedia Caballero, 1955; L. trini-
Travassos, 1914. Lauroiinae : cephalic cap not modified as three plates ; Male : posterior end relatively complex, with a gubernaeulum, relatively large number of caudal papillm and a well developed pre-cloacal sucker. Type species : P. uncinata (Rudolphi, 1819) Travassos, 1914. G e n u s I~ARASPIDODERA
REFERENCES. 1957. Sur la syst~matique des n~matodes du sous-ordre des Ascaridina parasites des vertebras. Bull. Soc. zool. Fr. 82, 243-253. FREITAS, J. F. T:EIXEII~A DE. 1956. l~otas sSbre " Heterakidae " Railliet & Henry, 1914 (Nematoda, Subuluroidea). Rev. 5rasil. Biol. 16, 461-482. INGLIS, WILLIAM G. 1957. The comparative anatomy and systematic significance of the head in the nematode family Heterakidae. Prec. zool. ~oc. Lend. 128, 133-143.
CHABAUD,fl~LAING.
