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A Revision of the Family Heteroderidae (Nematoda: Tylenchoidea) I

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A Revision of the Family Heteroderidae (Nematoda: Tylenchoidea) I A REVISION OF THE FAMILY HETERODERIDAE (NEMATODA: TYLENCHOIDEA) I. THE FAMILY HETERODERIDAE AND ITS SUBFAMILIES BY W. M. WOUTS Entomology Division, Department of Scientific and Industrial Research, Nelson, New Zealand The family Heteroderidae and the subfamilies Heteroderinae and Meloidoderinae are redefined. The subfamily Meloidogyninae is raised to family Meloidogynidae. The genus Meloidoderita Poghossian, 1966 is transferred to the family Meloidogynidae.Ataloderinae n. subfam. is proposed and diagnosed in the family Heteroderidae. A key to the three subfamilies is presented and a possible phylogeny of the family Heteroderidae is discussed. The family Heteroderidae (Filipjev & Schuurmans Stekhoven, 1941) Skar- bilovich, 1947 was proposed for the sexually dimorphic, obligate plant parasites of the nematode genera Heterodera Schmidt, 1871 and T'ylenchulu.r Cobb, 1913. Because of differences in body length of the female, number of ovaries, position of the excretory pore and presence or apparent absence of the anal opening they were placed in separate subfamilies; Heteroderinae Filipjev & Schuurmans Stek- hoven, 1941 and Tylenchulinae Skarbilovich, 1947. Independently Thorne (1949), on the basis of sexual dimorphism, proposed Heteroderidae to include Heterodera and Meloidogyne Goeldi, 1892; he considered the short rounded tail of the male and the absence of caudal alae as family charac- ters, and included Heteroderinae as the only subfamily. Chitwood & Chitwood ( 1950) ignored sexual dimorphism and based the family on the heavy stylet and general characters of the head and the oesophagus of the adults. They recognised as subfamilies Heteroderinae, Hoplolaiminae Filipjev, 1934 and the new subfamily Nacobbinae. Skarbilovich (1959) re-emphasized sexual dimorphism as a family character and stated that "It is quite illegitimate for the [previous] authors to assign the subfamily Hoplolaiminae to the family Heteroderidae". She placed in Heteroderidae all groups of nematodes with swollen females, including Hetero- derinae, with Heterodera as only genus, Tylenchulinae, Nacobbinae, Sphaeronema- tinae Raski & Sher, 1952 and the new subfamily Meloidogyninae. In the latter Meloidogyne and Meloidodera Chitwood, Hannon & Esser, 1956 were accom- modated. Paramonov (1967) agreed with Thorne's family concept, but recognized two different subfamilies: Heteroderinae and Meloidogyninae. It was Thorne's 1949 classification of the family Heteroderidae, with Hetero- derinae as the only subfamily, that became generally accepted (Franklin, 1971). Golden (1971) raised the family Heteroderidae to superfamily Heteroderoidea with families Heteroderidae and Nacobbidae. His classification of the family Heteroderidae is basically the same as the one proposed by Paramonov (1967) 440 except that besides Heteroderinae and Meloidogyninae a new subfamily Meloidode- rinae is recognized. Heteroderinae, with the genus Heterodera, is characterized by its potential to form a cyst. Meloidogyninae, with the genera Meloidogyne and Hypsoperine Sledge & Golden, 1964, is defined by a thin cuticle and the proximity of the vulva to the anus and their terminal position. Meloidoderinae, with the genera Meloidodera, Cryphodera and lVleloidoderita Poghossian, 1966, is based on the location of the vulva well removed from the anus. Wouts & Sher (1971) extended Thorne's definition of the family and recog- nized in it the subfamilies included by Paramonov (1967). The subfamilies were redefined and based on the location of the excretory pore in the female, the general shape and characters of the second-stage juvenile and the presence or absence of a stylet in the third- and fourth-stage juvenile. The ability to form a cyst was not recognized as a subfamily character. Heterodera, Meloidodera, Cryphodera Colbran, 1966 and two new genera, Atalodera and Sarisodera, were placed in Heteroderinae, while only the genus Meloidogyne was recognised in Meloidogy- ninae. Recently a new genus, closely related to Meloidodera and Cryphodera, was discovered in New Zealand. The three genera can be distinguished from all other genera in the subfamily Heteroderinae, sensu Wouts & Sher, 1971, by the annulated cuticle, which after death of the female does not become a cyst. This character is proposed as the basis for the subfamily Meloidoderinae. The genera and species of this subfamily will be further discussed in the next paper of this series. Of the other genera in the Heteroderinae, the genus Atalodera is characterized by the absence of annules on the female cuticle and its inability to form a cyst. The considerable differences between this genus and the genera in Meloidoderinae led Wouts & Sher (1971) to believe that several non-cyst forming, non-annulated forms emerged at this level of evolution of which, besides Atalodera, at least two other genera occur in Southern California. Atalodera therefore represents a group of undescribed genera so far known only from deserts in the south-western part of North America. This group is here proposed as a new subfamily, Ataloderinae. Heterodera, the type-genus and largest member of the family, and Sarisodera are at present the only two genera known to produce cysts and are retained in the subfamily Heteroderinae. The three subfamilies Meloidoderinae, Ataloderinae and Heteroderinae are closely related and are therefore considered to belong to one family, the Hetero- deridae. They are widely separated from Meloidogyninae which consequently is removed from Heteroderidae. The unique characters of Meloidogyninae make inclusion in other families of the Tylenchoidea impossible and it is therefore proposed as an independent family, Meloidogynidae. The species and genera of the different subfamilies of the family Heteroderidae will be further discussed in subsequent papers. The present paper serves to intro- duce and define Meloidogynidae and Heteroderidae and the subfamilies in the latter family. .
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