FNZ 55 - Criconematina (Nematoda: Tylenchida) - Introduction
Wouts, WM 2006. Criconematina (Nematoda: Tylenchida). Fauna of New Zealand 55, 232 pages.
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ISSN 0111-5383 (print),
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no.
55.
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Published 24 Mar 2006
ZooBank: http://zoobank.org/References/088E84BD-3DE3-4EA2-B6D9-C45BBC0A12F1
Introduction
Studies of plant nematode biodiversity in the past 40 years has demonstrated that species of the suborder Criconematina are disproportionately well represented in New Zealand. Over these years many new species were collected, and when I retired in 2001 a considerable number of these species were still undescribed. They are described in this work and combined with previously published information into a monograph on criconematids. This monograph should facilitate identification for the time being and form a solid base for future research on plant parasitic nematodes in New Zealand.
NEMATODES
Nematodes, or roundworms, are unsegmented, generally microscopic worms. Typically, their cuticle is transparent and internal structures can be observed through it. The digestive system is tubular with a buccal cavity anteriad, followed by the oesophagus, the intestine, and rectum, and the anus subterminally. There are females and males, their reproductive system consisting of one or two tubular gonads, but also hermaphroditism and parthenogenesis occurs. They comprise the phylum Nematoda.
In the humid New Zealand environment, the most commonly encountered and easiest to recognise nematodes are the mermithids. They parasitise insects, feeding on the fat body of the immature stage. Developing inside a host shorter than 5 cm, when they leave the insect mermithids may be longer than 30 cm. They mature in the soil, usually over a long period of time, and emerge during periods of prolonged rain. Crawling up on plants to lay eggs they can be easily seen with the naked eye.
Not all nematodes are parasites, as the majority of species are free-living. The plant and animal parasites together form a very large group, collectively capable of affecting almost all living organisms on earth. Vertebrate parasites can grow very long, the longest observed so far being 8 m, living in the placenta of sperm whales. Plant parasites are all microscopic in size.
Plant parasitic nematodes
In plant parasitic species the feeding stage is characterised by the presence of a stylet, a sharply pointed feeding tube in the buccal cavity, for piercing the wall of the host cell and feeding. Plant parasitic species are less numerous than free-living and animal parasitic species and have evolved in both the two classes of the phylum Nematoda, Cecernentia and Adenophorea.
In Adenophorea, plant parasitism is restricted to the families Trichodoridae (Diphterophorina, Dorylaimida) and Longidoridae (Dorylaimoidea, Dorylaimida). Species of these families can damage crops, but are better known for their ability to transmit plant viruses. Plant parasites of the class Cecernentia, generally known as the “true” plant parasites, are restricted to the order Tylenchida. All major plant damaging species belong to this taxon, including Criconematina.
Parasitic Tylenchida
In the order Tylenchida the females are generally less than 1 mm long and although typically slender they may be swollen to spherical in shape. Their stylet has evolved by transformation of the tissues of the wall of the mouth cavity, the stoma, and therefore is referred to as a stomatostyle. It is perfectly suited for puncturing the cells of plant roots. To facilitate passage of plant material through the narrow lumen of the stylet, on feeding the median bulb pumps digestive juices, excreted by the dorso-oesophageal gland, through the stylet into the plant cell for predigestion of the cell’s contents.
Plant parasitic nematodes need free water for locomotion and host finding. Below ground, within the soil environment, the relative humidity present at wilting point is more than adequate to allow movement. For survival in the absence of water and a host, plant parasitic nematodes have a survival stage. This survival stage may be the egg, any of the four juvenile stages, or the adult, depending on the species. The survival stage is capable of slowing down its metabolism and may be capable of anhydrobiosis. Because of this adaptability, damp soils, including rehydrated soils from the driest deserts, may be found teeming with nematodes. Typical survival stages are best known in non-criconematina. Tylenchs infecting above ground plant parts may survive for many years in their stored host. Cyst-forming species, in the absence of a host, may survive in soil for more than 10 years.
THE SUBORDER CRICONEMATINA
In Criconematina the procorpus and median bulb, the two anteriormost parts of the oesophagus, are amalgamated. In Criconematidae this amalgamated region surrounds the basal part of the retracted stylet with the stylet base residing in the middle of the median bulb. This gives the impression that the amalgamation of the anterior part of the oesophagus has provided the flexibility to accommodate and evolve long stylets — well over 100 µm in length in some species.The length of the female varies from about 200 µm to almost 2 mm and their shape from slender to spherically swollen. Transverse striation marks the cuticle. It may be very fine or extremely coarse. When coarse, it forms a distinct annulation on the cuticle, with the surface of the individual annules varying from smooth to extensively ornate. The cuticle of the body may have an outer layer that varies from a single thin sheath to a complete extra cuticle. Several of the species have an association with agricultural crops and some cause damage to crops. The majority of hosts, however, are shrubs and trees. Although several species are known from a single site only, the suborder generally is spread worldwide.
Earliest records in New Zealand
The genera Criconema Hofmänner in Hofmänner & Menzel, 1914, Criconemoides Taylor, 1936, and Macroposthonia de Man, 1880 have been recorded associated with agricultural crops since 1958 (Stout 1958, 1960; Clark 1963; Yeates 1967, 1968, 1974, 1975). Macroposthonia (= Mesocriconema Andrássy, 1965) xenoplax (Raski, 1952) De Grisse & Loof, 1965 was recorded from Prunus sp. (Dale 1972a) and grape (Grandison & Atkins 1985). Wouts (1966) described the first new species of the suborder, Paratylenchus halophilus. None of these species is considered endemic.
Endemism
That there are many endemic Criconematina species in New Zealand became clear in the 1970s. Raski and co-workers (Mehta & Raski 1971; Raski & Pinochet 1976) then reported on Criconematinae found in a collection of about 100 samples I had taken to the University of California, Riverside, in the late 1960s. They proposed the new genus Blandicephalanema Mehta & Raski, 1971 and described the new species B. serratum Mehta & Raski, 1971, B. pilatum Mehta & Raski, 1971, Ogma latens (Mehta & Raski, 1971) Raski & Luc, 1987, Criconema macilentum (Raski & Pinochet, 1976) Raski & Luc, 1985, C. pasticum (Raski & Pinochet, 1976) Raski & Luc, 1985, and C. spinicaudatum (Raski & Pinochet, 1976) Raski & Luc, 1985.
Colbran (1965), in Australia, had earlier described Pateracephalanema imbricatum (Colbran, 1965) Mehta & Raski, 1971, a species endemic to Australasia and also present in New Zealand. Loof et al. (1997) and Wouts (2000) added 12 Criconema species, and Wouts et al. (1999) added 6 Ogma Southern, 1914 species. All these species belong to the subfamily Criconematinae. Besides Criconematinae, Criconematidae contains the subfamilies Hemicriconemoidinae Andrássy, 1979 and Macroposthoniinae Skarbilovich, 1959, two subfamilies represented by the cosmopolitan species Hemicriconemoides cocophillus (Loos, 1949) Chitwood & Birchfield, 1957, Macroposthonia rustica (Micoletzky, 1915) De Grisse & Loof, 1965, and M. xenoplax. I am also including the native species M. campbelli sp. nov. in Macroposthonia. The position of M. campbelli sp. nov., however, is not certain: it may belong to Criconematinae.
Undisputed endemism of the suborder Criconematina is, therefore, restricted to the subfamily Criconematinae. Within Criconematinae it is confined to the genera Blandicephalanema, Criconema, Ogma (= Crossonema Mehta & Raski, 1971), and Syro Orton Williams, 1985. Bakernema Wu, 1964, Lobocriconema De Grisse & Loof, 1965, and Neolobocriconema Mehta & Raski, 1971, the other 3 genera in Criconematinae, are not represented in New Zealand.
Blandicephalanema (= Amphisbaenema Orton Williams, 1982) and Syro species are restricted to the South Pacific region. With the addition of 2 new species to each genus, 6 nominal Blandicephalanema, including 4 endemic, and 3 Syro species, including 2 endemic, are now known.
Criconema and Ogma are distributed worldwide. The 4 new Criconema species described here bring to about 100 the number of species recognised in the genus, 19 being endemic to New Zealand. The 6 new Ogma species described here bring to 60 the total number of species recognised in this genus, 15 of which are endemic to New Zealand. The other 5 Criconema and 7 Ogma species known from New Zealand are considered introduced by humans over the last 200 years.
The 47 Criconematinae, including 40 endemic species, known from New Zealand, outnumber the mere 34 West-European, including just 7 Criconema and 8 Ogma species (Siddiqi 2000; Wouts & Sturhan 1999), by almost 50%. The actual difference is probably much greater, with the European species being collected exhaustively and the New Zealand species originating from limited collections, with many species probably still undiscovered.
PLANT NEMATOLOGY IN NEW ZEALAND
Clark (1963) gives a detailed account of the early development of plant nematology in New Zealand. As the first contribution to nematology he recognised Kirk’s (1899) advisory leaflet for farmers on wheat cockle eelworm, Anguina tritici (Steinbuch, 1799) Dujardin, 1845. Kirk’s subsequent reports in the Annual Reports of the Department of Agriculture of 1903 and 1907 of tubers of potatoes being attacked by a population of root-knot nematodes (Meloidogyne Goeldi, 1892) were misidentifications according to Clark (1963), the real cause being a combination of Meloidogyne sp. and Ditylenchus destructor Thorne, 1945.
A comprehensive list of plant parasitic nematodes first appeared in the Annual Report of the Department of Agriculture of 1908. A year later Kirk & Cockayne recorded root knot nematodes from cucumbers and tomatoes, and the beet cyst nematode, Heterodera schachtii Schmidt, 1871, from a local crop of mangold (Clark 1963). The next period of 25 years yielded no further records on nematodes.
In 1935 Reid & Cottier recorded Aphelenchoides ritzemabosi (Schwartz, 1911) Steiner, 1932 on chrysanthemum, and in 1937 Muggeridge & Cottier reported it causing death of black currant buds. Field trials with root knot nematode species on tomatoes, starting in the early 1940s, were reported by Jacks (1944, 1945, 1948, 1963) and Stanton (1956). Blair & Morrison (1949) reported on Anguina tritici, Ditylenchus dipsaci (Kûhn, 1857) Filipjev, 1936 and Meloidogyne sp. on wheat and oats, and Cottier (1956) published a summary of plant parasitic nematodes of New Zealand. Clark (1963) published the first authoritative list of plant parasitic nematodes. It contained 11 genera, 4 with no species, 3 with a single species, and 4 with 2 species. Updated by Dale (1972a), it increased to 14 genera, each with at least 1 species, and a total of 27 species including 4 virus-transmitting species. Knight et al. (1997) listed 31 genera, 4 without named species, totalling 78 species including 10 virus-transmitting ones. The increase in the total number of nematodes identified from New Zealand, including free-living and marine forms, was even more dramatic. Yeates (2005) listed more than 500 species in almost 300 genera.
The upsurge of new records of nematode species, and species descriptions, from New Zealand since the 1960s is the result of the fulltime employment of nematologists since then. The withdrawal of public funds in the early 1990s, when the government introduced its user pays policy, however, has caused a gradual reduction in nematological studies. Only ecological studies are continuing presently as nematological activities.
THE ORIGIN OF THE NEW ZEALAND NEMATODE FAUNA
The generally high relative humidity provides an environment ideally suited for the survival and development of plant parasitic nematodes. In agricultural crops cosmopolitan species are primarily represented. The abundance of different habitats in New Zealand and the resulting survival and evolution of a wide diversity of native plant species have enabled the development of many endemic plant-parasitic nematode species. Of special interest among them are species with a strong lineage with species evolved in neighbouring countries and continents. It has long been recognised that in Radopholus Thorne, 1949 (Pratylenchidae: Hoplolaimina) a strong lineage exists with Australian species, the genus being nearly restricted to these two countries except for some cosmopolitan species (Sher 1968). Similarly, in the genus Globodera (Heteroderidae: Hoplolaimina) a lineage seems to exist with South America where the Chilean Andes is postulated to represent the centre of origin (Mai 1977). Globodera zelandica Wouts, 1984 was described from New Zealand where infective juveniles and cysts of further species of the genus have been found in a variety of habitats, including subalpine regions. This general presence of Globodera species in New Zealand hints at their common ancestry with Globodera species from South America originating in Gondwanaland.
Among the Criconematina from New Zealand there is a strong lineage with both Australian and South American species. Species from the subantarctic islands associated with trees especially show a striking similarity with those from Southern Chile. A key factor in the parallel development of nematode species in South America and Australasia is the tenacity of their common or related ancestral hosts. They freely colonised our part of Gondwanaland, evolving in the process and allowing nematode species to evolve with them. Continental drift caused further spatial separation and the evolution into related, but different species in South America, New Zealand, and Australia, and in some of the much smaller island fragments of the South Pacific.