JOURNAL OF NEMATOLOGY VOLUME 25 SEPTEMBER 1993 NUMBER 3 Journal of Nematology 25(3):315-331. 1993. © The Society of Nematologists 1993. Feeding Habits in Soil Nematode Families and Genera--An Outline for Soil Ecologists G. W. YEATES, 1 T. BONGERS,2 R. G. M. DE GOEDE, 3 D. W. FRECKMAN, 4 AND S. S. GEORGIEVA5 Abstract: Because research on nematode involvement in trophic interactions, foodweb structure, and biodiversity is constrained by lack of an overview of nematode feeding habits, this outline presents a consensus of current thought on nematode feeding habits. The source of food is funda- mental to trophic interactions and provides the basis for our definitions of the essential feeding types: 1) plant feeder, 2) hyphal feeder, 3) bacterial feeder, 4) substrate ingester, 5) predator of animals, 6) unicellular eucaryote feeder, 7) dispersal or infective stage of parasites, and 8) omnivore. Lists of families and genera with their presumed feeding types are given. Major gaps in knowledge of feeding in the smaller tylenchids and many dorylaims are noted. Key words: bacterial feeding, feeding habit, foodweb, fungal feeding, nematode, omnivore, pred- ator, soil ecology, trophic interaction. With the increasing interest of soil ecol- there will follow a better understanding of ogists in the role of nematodes in ecosys- the role of nematodes in soil and how tem processes (roles such as nutrient cy- changes in environmental factors influ- cling, biological control and economic crop ence the composition of the nematode loss), there is an unmet need for a concise fauna. summary of current knowledge of nema- The first comprehensive review of tode feeding habits. The analysis of avail- nematode feeding habits was given by able information is made increasingly dif- Neilsen (77). In an attempt to produce ficult by changes in nematode systematics functional groups based on feeding habits, and recent contributions to nematode ecol- Paramonov (84) applied to nematodes ogy. When all species of nematodes can be terms such as "pararhizobes" (occur in the confidently assigned to feeding groups, rhizosphere and sometimes damage plants) and "dyssaprobes" (feed in decom- posing material but may enter healthy tis- Received for publication 12 January 1993. sue). Both Wasilewska (121) and Yeates Review. (127) grouped plant and soil nematodes by z Landcare Research, Private Bag 31902, Lower Hurt, New Zealand. feeding habits. The classification of Ty- 2 Nematology Department, Wageningen Agricultural Uni- lenchida advocated by Siddiqi (99) has a versity, P.O.B. 8123, 6700 ES Wageningen, The Nether- lands. strong "feeding habit" component. Recent 3 Biological Station of Wageningen Agricultural Univer- ecological studies have revealed that feed- sity, Kampsweg 27, 9418 PD Wijster, The Netherlands. Department of Nematology, University of California, ing-habit groupings may not be sharply Riverside, CA 92521. Present Address: Natural Resource delimited. For example, abundant popula- Ecology Laboratory, Colorado State University, Fort Collins, CO 80523. tions of Aphelenchoides, Tylenchus, Tylen- 5 Nematology Laboratory, Department of Zoology, Faculty cholaimus, and Ditylenchus were discovered of Biology, University of Sofia, Sofia 1421, Bulgaria. We are grateful to B. Sohlenius, V. R. Ferris, D. C. Cole- that could only be classified as "root/fungal man, S. Bostrom, R. K. Niles, K. Prejs, D. Wardle, and P. feeding nematodes" (105), as well as "pre- Arpin for their comments on the manuscript, and to D.J. Carlisle, E. M. Courtright, and T. Gates of D.W.F.'s lab for dacious" mononchids that multiplied using proofreading and library research. Support from the Foun- bacteria as a food source (130). These ex- datiott for Research, Science and Technology (NZ) to G.W.Y. and from the National Science Foundation (USA) Grant BSR amples demonstrate the apparently arbi- 8818049 to D.W.F. is gratefully acknowledged. trary nature of traditional nematode feed- The JOURNAL OF NEMATOLOGY for June (25:101-313) was 315 issued 11 June 1993. 316 Journal of Nematology, Volume 25, No. 3, September 1993 ing groups. Moreover, feeding habits of 1. Although normally regarded as bac- many nematodes have been inferred terial feeders, Chiloplacus (Acrobelidae) rather than confirmed by maintenance and Rhabditis (Rhabditidae) have been cul- over many generations under biologically tured on the fungi Phoma sp. and Pythium defined conditions. middletonii, respectively (39,92). In both Following Petersen and Luxton (86), we cases, the "primary" food source is bacte- use "grazing foodweb" and "detritus food- rial; the fact that the apparent secondary web" as terms for communities based on food belongs to the same trophic level of living green plants and dead organic mat- the "detritus foodweb" as the primary food ter, respectively. Their comments on the shows the value of acknowledging such merging of the two webs are particularly broad foodwebs. However, our interpreta- relevant for nematodes, which are so often tion of this dual feeding habit is i) bacterial abundant at interfaces between living and contamination of the nematode cultures or dead material (as in the rhizosphere). ii) direct uptake of nutrients by nema- This paper is not a literature review and todes, as occurs in axenic culture of Cae- does not present new results; rather we norhabditis elegans (21,70,132). present a basis for advancing understand- 2. Hooper and Cowland (45) cultured ing of the role of nematodes in soil ecol- the foliar nematode Aphelenchoides ritzema- ogy. The paper originated in discussions at bosi, which normally feeds in the "grazing the Second International Nematology foodweb," on fungi ("detritus foodweb"), Congress and lists nematode families and reinforcing observations that fungal feed- genera with our assessment of current un- ing is the normal situation in Aphe- derstanding of their feeding habits. We lenchida. Just as plant root cells are fed on hope that this paper will serve as a frame- in a variety of ways (see "plant feeding"), so work for ecologists to use independently of are fungi (1). taxonomic philosophies. Andr~ssy (2,3), 3. It is difficult to extrapolate data from Ltrenzen (58), Maggenti (62), and Siddiqi closely controlled monoxenic cultures of (99) all have differing approaches to the Pratylenchus and Radopholus on carrot discs general classification of nematodes. The to the heterogenous environment of field most recent taxonomic overview is con- populations. tained in the Manual of Agricultural 4. Although certain mononchids suc- Nematology (76). The generic makeup of cessfully cultured on bacteria contain liv- the families we use is compatible with these ing bacteria within the intestines (6), we recent works; because they often assign question whether sufficient aggregations differing taxonomic ranks to these groups, of bacteria exist under field conditions for we do not list authorities. bacterial ingestion to be of significant nu- tritional importance to the large monon- CONFLICTING RESULTS AND OBSERVATIONS chids. 5. The intestine of mononchids, rhab- Soil ecologists are primarily concerned ditids, dorylaims, etc., often appear pig- with relationships between biological pop- mented, but such pigmentation has not utations and the soil environment, whether been observed in Tylenchida or plant- it be a high-input agroecosystem, natural feeding Trichodorus and Longidorus (76). ecosystem, or an area managed for sus- There has been no attempt to relate this tained production. When these popula- pigmentation to feeding habits. tions are cultured singly or together in the 6. Axenic culture of Caenorhabditis ele- laboratory, many possible interactions and gans and other "bacterial feeding" nema- their consequences are reduced (52); thus, todes (21,70,73,132) highlights problems results are difficult to extrapolate to field of interpretation, but there is evidence that conditions. The following are examples of development may be slower under axenic such difficult extrapolations. conditions (20). Bacterial feeding is re- Feeding Habits of Soil Nematodes: Yeates et al. 317 garded here as the principal source of nu- species, the feeding site of the female may trition for such nematodes under field be undifferentiated, uninucleate, or poly- conditions. Physical crushing of bacteria nucleate. Males of sedentary species some- has been demonstrated in the pharyngeal times have a degenerate stylet or reduced bulb of Acrobeloides nanus, but bacterial oesophagus, but data on the nutrition of feeding nematodes may defecate living such males is inadequate. Plant feeders bacteria and there is no general knowledge may be polyphagous or show host specific- as to whether some nematodes actually kill, ity. Migratory species may generally be rupture, or lyse bacteria or merely remove classified as ecto- or endoparasites. Feed- adhering organic compounds (126). In ing sites may be root-hair, epidermal, cor- several situations, there may be a degree of tical, or vascular. direct nutrient uptake through the cuticle Although apparently not actively feed- or epidermis (33,50,79,132). ing, the migratory phases of Pratylenchus, 7. Although identification to family infective second-stage Heterodera, and re- level is usually adequate, identification to sistant stages of Paratylenchus are each an species is sometimes necessary to accu- essential part of the life-cycle of these ob- rately assign nematodes to trophic groups. ligate plant feeders and are thus included For example, Ditylenchus dipsaci is an eco- in