Plant-Parasitic Nematodes: A Pictorial Key to Genera [Fifth Edition] 9781501728419

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PLANT-PARASITIC NEMATODES

PLANT-PARASITIC NEMATODES A

PICTORIAL

KEY

TO

GENERA

FIFTH EDITION

William F. Mai and Peter G. Mullin Howard H. Lyon

AND

Kent Loeffler,

wrTH

PHOTOGRAPHERS

COMSTOCK PUBLISHING ASSOCIATES CORNELL UNIVERSITY PRESS I

A DIVISION OF

ITHACA AND LONDON

Copyright© 1960 by W. F. Mai and H. H. Lyon First Revision, 1962 Second Revision, 1964 Supplement to Second Revision, 1966 Third Revision, 1968 Fourth edition, revised, © 1975 by Cornell University Fifth edition, copyright© 1996 by Cornell University All rights reserved. Except for brief quotations in a review, this book, or parts thereof, must not be reproduced in any form without permission in writing from the publisher. For information address Cornell University Press, Sage House, 512 East State Street, Ithaca, New York 14850. First published 1996 by Cornell University Press

Printed in the United States of America

Library of Congress Cataloging-in-Publication Data Mai, W. F. Plant-parasitic nematodes : a pictorial key to genera I William L. Mai and Peter G. Mullin ; with Howard Lyon and Kent Loeffler, photographers. -5th ed. p. em. Rev. ed. of: Pictorial key to genera of plant-parasitic nematodes. 4th ed. 1975. Includes bibliographical references (p. ) and index. ISBN 978-0-8014-3116-6 (cloth: alk. paper) 1. Plant nematodes-Identification. 2. Plant parasites--Classification. I. Mullin, Peter G. II. Mai, W. F. Pictorial key to genera of plant-parasitic nematodes. III. Title. QL39l.N4M22 1996 595.1 '82-dc20 95-24787 Cornell University Press strives to use environmentally responsible suppliers and materials to the fullest extent possible in the publishing of its books. Such materials include vegetable-based, low-VOC inks and acid-free papers that are recycled, totally chlorine-free, or partly composed of nonwood fibers. For further information, visit our website at www.cornellpress.cornell.edu. Cloth printing

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Contents

Preface

vii

Key to Genera of Plant-Parasitic Nematodes (without Pictures)

1

Key to Genera of Plant-Parasitic Nematodes (with Pictures)

7

Natural Classification Schemes for Plant-Parasitic Nematodes

166

Classification of Phylum Nemata

167

Classification of Aphelenchida

168

Classification of Tylenchida

170

Classification of Dorylaimida and Triplonchida

174

Addendum: Selected References to Genera of Nematodes Not Included in the Key to Genera (with Pictures)

181

General References

198

Selected References

200

Glossary of Nematological Terms

266

Index to Genera and Subgenera

271

Preface

Nematodes, perhaps the most numerous of the multicellular animals, can be found in almost all environments-from hot springs to the frozen Arctic and Antarctic. Many are damaging parasites of plants and animals, including humans, and cause some of the world's most serious diseases. Nematodes are also beneficial. In agricultural soils, many and varying kinds of nematodes are antagonistic to, and help control, organisms that cause important plant diseases. And nematodes have shown promise as a means of managing some difficult-tocontrol insects such as black flies. A nonparasitic nematode, Caenorhabditis elegans, has played a key role in the investigation of basic biological systems such as embryological development. In most nematological research, whether of harmful or helpful species, it is essential to be able to accurately identify the nematodes involved. This pictorial key is intended primarily for the use of students and others who wish to identify nematodes. As nematode taxonomy becomes increasingly complex, the greater is the need for students to begin studying the systematics of these ·organisms. This book, with its descriptive key, accompanying photographs and drawings, generic descriptions, and one or more paragraphs listing the characteristics of each genus will help students learn to differentiate plantparasitic nematodes from other types of nematodes that occur in soil and in plant tissue and to identify the plant-parasitic nematodes to genus. (Although an initial determination as to genus may be made on the basis of the key and illustrations, the descriptions and characteristics should always be considered before assigning a nematode to a particular genus.) To identify species within a genus, one will need to consult one or more of the taxonomic publications listed in the Selected References for that genus; the publications that contain keys to species are marked with an asterisk. Included in the pictorial key are most of the genera that have plant-parasitic species. Several genera found near plant roots, but not proven to be parasites of plants, are included because of their close relationship to plant-parasitic species of other genera. Also included are genera such as Psilenchus that, although not known to be parasitic on higher plants, often are found in large numbers in soil samples taken from around plant roots.

More than 200 genera of known or suspected plant-parasitic nematodes have been described in the literature since 1975, when the fourth edition of the Pictorial Key to Plant-Parasitic Nematodes was published. Two of them, Bursaphelenchus and Globodera, are described in detail in this fifth edition, and two substitutions have been made. Paratrichodorus has been inserted in place of Trichodorus, because many of the damaging stubby root nematodes are classified in Paratrichodorus at present. The genus Tetylenchus, which at this time is of uncertain taxc onomic position, has been replaced by Merlinius, a genus more widely accepted and more likely to be encountered by nematologists examining soil samples. We decided not to include more of the genera described in the past twenty years because we felt that the addition of a large number of genera would result in an unwieldy key, one that would be too confusing for beginning students to use. Publications on selected recently described genera not included in the pictorial section of the key are listed in the Addendum. The key used in this book is based largely on morphological characters of mature females. Males and juveniles can be used to verify an identification, but only adult females should be used to positively identify a nematode to genus. The techniques used to extract nematodes from soil and plant parts and to prepare them for observation can greatly alter these specimens, making identification easy or difficult. For example, in centrifugal flotation extractions, certain kinds of nematodes will shrink if immersed for extended periods in sugar solutions. The appearance of specimens may also be influenced by the care they receive before, during, and after extraction; in general, exposure to high temperatures, desiccation, and storage in water for a long period before killing reduce the lifelike appearance of nematodes. Specimens recently killed by gentle heat (65°C for two minutes) and mounted in water appear more lifelike, permitting better observation of characters, than do killed and fixed specimens, particularly those mounted in glycerine. In temporary or permanent mounts, the omission of coverslip supports may result in the flattening of a specimen and thus change measurements of taxonomic characters. Because of the considerable variation in morphology among individuals of the same genus, or even species, and the

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viii

Preface difficulty in observing taxonomic characters of certain specimens, at least four to six individuals should be observed before making a positive identification. Techniques for the extraction of nematodes from soil or plant parts, killing, fixing, and preparing temporary and permanent mounts are given in the manual edited by J. F. Southey (1986). In addition to the pictorial key, this publication provides further information related to nematode taxonomy, including a descriptive key without pictures. When taxonomic characters are thoroughly understood so that pictures are not needed, identification to genus can be made more rapidly with the descriptive key than with the pictorial key. The literature citations for each genus are listed alphabetically by author in the Selected References. Approximately 2500 references are listed. Also included is a list of general references on the taxonomy and morphology of nematodes, particularly of plantparasitic nematodes, and techniques related to identifying them. Most of the publications included are relatively recent. Certain recently described or rare genera found around plant roots, especially those difficult for a student to differentiate from more widely distributed or economically important genera, are listed in the Addendum rather than in the pictorial key. Some of these genera have been widely accepted by nematologists, but the validity and placement of others remain subjects of discussion. We have selected a single reference for many of the genera included in the Addendum to give the user a starting point for entry into the literature. Some of these additional genera are also discussed briefly in the General Characteristics sections of genera to which they are considered most closely related. Although generic descriptions are omitted, publications concerning these genera may be found in either the Selected References under the related genus or genera or the General References. A glossary of nematological terms has been included to help users of the pictorial key understand the characters defined. The index makes it possible to locate the picture of a representative of a particular genus, the description and general characteristics of the genus, and a list of publications about the genus. The characters used in the pictorial key to separate genera are those considered to be most easily distinguishable by students. Light and scanning electron micrographs have been included to help students visualize certain characters.

Because the organization of this key is based primarily on characters judged to be most easily observed by students, related nematode genera may not appear together. Four relatively recent classification outlines are included to provide some information on the natural relationships of nematodes: an outline of the phylum Nemata (Maggenti, 1981), a proposed scheme for the order Aphelenchida (Hunt, 1993), a classification scheme for the order Tylenchida (Ebsary, 1991), and an outline of the orders Dorylaimida and Triplonchida (Jairajpuri and Ahmad, 1992). Numerous other classification schemes have been proposed that differ to a greater or lesser extent from those included in this book. Several of the sources listed in the General References contain information on nematode classification, and the reader is encouraged to consult those as well. Part of the descriptive key is based on "A Key to the Mature Females of the Tylenchoidea," an unpublished paper prepared by A. L. Taylor. Terms and definitions included in the Glossary were taken from lists prepared by H. J. Jensen and by H. Triantaphyllou and K. R. Barker, as well as from A Glossary of Nematological Terms by F. E. Caveness (1964). Permission to reprint line drawings and photographs that have been previously published is gratefully acknowledged; specific acknowledgments are given in the plate legends. Howard Lyon prepared the lifelike photographs of recently relaxed specimens that have been integral to all the editions of this work. The substantial contributions of Barbara Mullin in locating, accumulating, and organizing information published in the literature since 1975 were crucial to the production of this volume. The valuable assistance of Terry Costigan, Tamara Clark, Charlotte Stahl, and Louis Hsu in preparing reference lists, checking literature citations, compiling the text, and helping in innumerable other ways is greatly appreciated. The role of John M. Ferris in reviewing the key and making suggestions is also gratefully acknowledged. Without the expert word processing of Mary Brodie, the early and final drafts of this edition would not have been possible. This important contribution is here recognized and gratefully appreciated. WILLIAM PETER

Ithaca, New York

G.

F. MAl

MULLIN

PLANT-PARASITIC NEMATODES

Key to Genera of Plant-Parasitic Nematodes (without Pictures) (Based mainly on characteristics of adult females)

la. lb.

Stylet absent. ....................................................... Not a plant parasite Stylet present ...................................................................... 2

2a.

Two-part esophagus, no valvulated apparatus, anterior part slender, posterior part glandular and muscular; stylet usually without basal swellings [Order Dorylaimida] .............................. 3 2b. Three-part esophagus usually with a valvulated metacorpus (median bulb) followed by a slender isthmus and glandular basal bulb; stylet usually with basal knobs [Orders Aphelenchida and Tylenchida] ............................................................................ 6 3a. Stylet short, curved; body short and thick (0.45-1.5 mm long) ................. Paratrichodorus 3b. Stylet long, straight, tapering to a long slender point with long extensions; body long and slender. .............................................................................. 4 3c. Stylet straight, usually not very long (includes numerous genera of uncertain feeding habits; group contains no known plant pathogens) ............................... A large number of genera 4a.

Stylet extensions with sclerotized basal flanges; guiding ring near base of stylet just anterior to junction of stylet and stylet extensions ................................................. Xiphinema 4b. Stylet extensions without basal flanges; guiding ring near apex of stylet ...................... 5 5a.

Amphid openings minute, slitlike; amphids consisting of large pouches that almost encircle the head ......................................................................... Longidorus 5b. Amphid openings wide, sublabial, extending at least halfway across the neck at that point; amphid pouches funnel- to stirrup-shaped .......................................... Paralongidorus 6a.

Dorsal esophageal gland outlet in metacarpus, anterior to valve, or in that position when median bulb absent (usually difficult to see); metacarpus very large, often appears nearly as wide as the diameter of the body [Order Aphelenchida] ........................................................ 7 6b. Dorsal esophageal gland outlet in procorpus (usually can be seen more readily in recently prepared water mounts than in glycerine mounts); metacarpus moderate to reduced in size (less than threefourths body width) [Order Tylenchida] ................................................. 9 7a. Vulval flap absent; vagina normal; a (body length I greatest body width) less than 80 ........... 8 7b. Vulva with wide overlapping flap; vagina curved; a around 100 ............. Rhadinaphelenchus 7c. Vulva with overlapping flap; male with large spicules, arcuate, paired, with sharply pointed rostrum and disclike expansions; a around 40 ......................................... Bursaphelenchus 8a.

Tail of female blunt; lateral field with 6-14 incisures; male with bursa and gubernaculum ... ~ ..... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . , ........................... Aphelenchus 8b. Tail of female usually conoid, often with one or more sharp points at the terminus (mucronate); lateral field with two to four incisures; male without bursa or gubernaculum ............ Aphelenchoides

9a. Head with setae; no plant parasites ................................. Atylenchus, Eutylenchus 9b. Head without setae; numerous plant parasites ........................................... 10 lOa.

Metacorpus absent or reduced; if reduced, no sclerotized valve .......... Examples: Nothanguina, N othotylenchus lOb. Metacarpus with sclerotized valves present (usually can be seen more readily in recently prepared water mounts than in glycerine mounts) ..................................................... 11 1

2 Key to Genera lla. 11 b.

Mature females greatly enlarged (pear-shaped, lemon-shaped, kidney-shaped, or saccate); found in roots of plants either embedded or attached by neck; some occur as cysts in soil .............. 12 Mature females vermiform; may be slender to slightly swollen ............................. 23

12a.

Mature females soft, elongate-saccate, or kidney-shaped with tail (except for Sphaeronema, which is spherical without a tail) ............................................................. 13 12b. Mature females becoming cysts or remaining soft-bodied; pyriform-saccate, spheroid, or lemon-shaped, usually without a tail ............................................................... 18 13a. Mature female with two ovaries ............................................ Rotylenchulus 13b. Mature female with one ovary ....................................................... 14 14a. Excretory pore located in normal position, near nerve ring ................................ 15 14b. Excretory pore located posterior to nerve ring ........................................... 16 15a.

Mature female subspherical; cuticle marked with coarse reticulate pattern; may have a prominently protruding vulva, subterminal in position ..................................... Sphaeronema 15b. Mature female spiral, thickened; without protruding vulva ........................ Trophonema 16a. Circumoral elevation present in females and juveniles ...................... Trophotylenchulus 16b. Circumoral elevation absent ......................................................... 17 17a. Excretory pore near vulva ................................................... Tylenchulus 17b. Excretory pore located near basal region of esophagu_s ............................. Nacobbus 18a.

Females with irregular body annules around perineum (perineal pattern); excretory pore at level with stylet or close behind it; lip region with two lateral lips wider than four sublateral lips; second-stage juvenile stylet 20 !Jom; well-developed labial framework; usually no galling of host roots ...................... 19 19a. 19b.

Vulva subequatorial; cuticle annulated ........................................ Meloidodera Vulva terminal or subterminal; cuticle annulated or lacelike ............................... 20

20a. Cuticle annulated .......................................................... Cryphodera 20b. Cuticle with lacelike pattern ......................................................... 21 21a.

Cyst stage present; vulva terminal, anus dorsal, not on vulval lip; or vulva sunken into terminal vulval cone with anus on upper inside of dorsal vulval lip ...................................... 22 2lb. No cyst stage; vulva and anus terminal on prominence ............................. Atalodera 21c. No cyst stage; vulva sunken into terminal vulval cone; anus on upper inside of dorsal vulval lip; secondstage juvenile stylet >38 !Jom ................................................. Sarisodera 22a.

Cysts generally lemon-shaped, rarely spherical and then with buttonlike protrusions; vulva on a terminal cone, with fenestration (circumfenestrate, bifenestrate, or ambifenestrate); bullae present or absent; stylet