Soil Nematodes in Terrestrial Ecosystems ~ G

JOURNAL OF NEMATOLOGY VOLUME ll JULY 1979 NUMBER 3

Soil Nematodes in Terrestrial Ecosystems ~ G. W. YEATES 2

Abstract: There has been much work on plant-feeding nematodes, and less on other soil nematodes, their distribution, abundance, intrinsic properties, and interactions with biotic and abiotic factors. Seasonal variation in nematode fauna as a whole is correlated with factors such as moisture, temperature, and plant growth; at each site nematode distribution generally reflects root distribution. There is a positive correlation between average nematode abundance and primary production as controlled by moisture, temperature, nutrients, etc. Soil nematodes, whether bacterial feeders, fungivores, plant feeders, omnivores, or predators, all influence the populations of the organisms they feed on. Ahhough soil trematodes probably contribute less than 1% to soil respiration they may play an important role in ntttrient cycling in the soil through their influence on bacterial growth and plant nutrient availability. Key Wo~ds: ecology, energetics, microcosms, nutrient cycling, primary production.

Nematodes, as one component of the soil nematode populations are more likely to be ecosystem, interact with biotic and abiotic ill equilibrium, albeit dynamic, with their factors, producing economic crop losses enviromnent, than in cultivated fields where but also having many other effects, largely conditions are subject to more drastic unknown. The role of the nematode com- changes. In interpretation, however, knowl- munity in ecosystems is essential knowledge edge of plant nematode biology and for managing plant nematode populations interactions derived from agriculture are (42), clarifying the role of nematodes in nsed. dispersing algae, fungi, bacteria, phages, and Nematodes feed on a wide range of viruses (103, 104), decreasing energy inputs foods, and this paper uses the following to farming, disposing of organic wastes (57), trophic groups: bacterial feeders, fungivores, and dealing with nematode tolerance to plant feeders, onmivores, predators. In nematicides (80). Keys to understanding interpreting interactions, feeding and para- that role will be knowledge of the dis- sitism should be distinguished (109) as well tribution and diversity of nematodes in as parasitism and pathogenicity (95). Soil ecosystems, as well as their popnlation samples may also yield soil stages of nema- dynamics and their influence on food todes that parasitise invertebrates and sources. vertebrates. This paper, concerned mainly with Any study of nematode populations, nematodes in natural or lightly managed which repeated sampling has shown to con- terrestrial ecosystems, relies heavily on data lain up to 105 species (41) and 29,800,000 collected from such habitats during tile individuals per m'-' (94), must take into International Biological Programme (1964- consideration the distribution in time and 1974). The role of nematodes in ecosystems space not only of the nematodes but also of is understood more easily, and sampling factors which may interact with them. The effort reduced, in stable habitats where way in which each variable is measured may be crucial. There are many methods of extracting nematodes, each with its own Received for publication 10 July 1978. efficiency (7), and ecologists have an added a Invitational review. This review was completed while on study leave in the Nematology Department, Rothamsted problem of assessing whether the nematodes Experimental Station, Harpenden, Herts., England, during recovered were active at the time of sam- tenttre of a Nuflield Foundation Commonweahh Travelling Fellowship. I thank Drs. B. Sohlenins and J. D. Stout for pling so their metabolic contribution may comments. be assessed (29, 64, 79). The typical ag- ~Soil Bureau, D.S.I.R., Private Bag, Lower Hutt, New Zealand. gregated distribution of all plant and soil

The JOURNAL OF NEMATOLOGY for April (ll: 1 17-212) was issued 27 April 1979. 218 214 Journal o[ Nematology, Volume 11, No. 3, July 1979 nematode populations necessitates repli- forests and temperate grasslands have sim- cated sampling. Some nematologists work ilar densities. Nematodes from deciduous with individual cores (41, 110) and some forests and temperate grasslands are also bulk cores for extraction of subsamples similar in total dry biomass and mean in- (102); results are normally expressed per m"- dividnal biomass, although considerably to a specified sampling depth, with some greater than nematodes from evergreen estimate of variability. Biomass and dry forests. Acid conditions prevailing in weight are often calculated so the respira- coniferous forest soils are inimical to tory activity and calorific content of the lumbricid earthworms, millipedes, and nematodes may be assessed and related to woodlice, but soil fungi flourish much ecosystem dynamics. better than in looser base-rich soils of deciduous stands. In evergreen coniferous POPULATION SIZE, STRUCTURE, forests, fungal-feeding Tylenchida are likely AND DIVERSITY to become more numerous; their small size is partly responsible for the smaller biomass Nematodes in differing ecosystems: in such forests. Nematode abundance and biomass from 115 Table 1 gives hourly respiratory rates at places and habitats, including published 2 C. In tundra the temperature is limiting and unpublished International Biological for much of the year, whereas in deserts Programme data, show: anhydrobiosis would be important. On an 1) Population estimates range from annual basis the more equitable micro- 8,100/m'-', for rain forest in Puerto Rico, to climate in evergreen forests probably offsets 30,000,000/m 2 for meadow steppe in the the lower hourly respiratory rate: annual USSR (69). values are probably similar for temperate 9) Wooded and non-wooded ecosystems grasslands, evergreen forests, and deciduous have similar population ranges. In non- forests. wooded habitats, mean nematode popula- The ratio between maximum and min- tion densities tend to fall in the series mesic inmm nematode population densities over >wet >dry, and, when separated by the the year varies from 2x for an English degree of organic matter on the soil surface, beech woodland (71), 3× for a New Zealand mineral soils have higher densities than or- sand dune (106), 4× for a French grassland ganic mors and peats (69). (11), 5x for English moorland (6) and 3) The relationship between abundance Danish beech forest (110), 6× for Finnish and dry weight snggests that mean imti- spruce (38) and Swedish pine forests (82), vidual biomass is greater for grassland to 10× for a grazed New Zealand pasture nematodes than for woodland nematodes (117). In part this reflects climatic differ- (69). ences, but nematodes are a component of 4) Nematode abundance and average in- ecosystems in which there are daily, sea- dividual weights appear lower for temperate sonal, and annual fluctuations around the coniferous forests than for deciduous forests 'maximmn persistent biomass', which itself (69). is less than the 'maximum potential bio- Table 1 summarises data for 28 sites at mass', depending on the severity of the which I have judged sampling to be ade- habitat. quate to calculate an annual mean popula- Nematodes in climatic and vegetational tion; use of annual means greatly reduces sequences: Studying nematode populations mean populations in grasslands (7,200,000 in a sequence in which the climate, soil, or to 1,900,000/m ~) and deciduous forests vegetation is constant is useful in illustrat- (6,100,000 to 1,700,000/m 2) compared with ing the effect of these factors on population those given by Petersen (69). Although composition and species ecology. based on a single site, deserts clearly have Nematodes at six sites, with soils from lower nematode density than other eco- similar parent material, supporting tussock systems. Petersen (69) had the impression grassland under precipitation of 350-5000 of greater nematode abundance in decidu- ram, were investigated using autumn sam- ous than in evergreen forests; annual means ples (113). Total abundance declined with show no significant differences. Deciduous altitude, whereas diversity did not. Para- TABLE 1. Average nematode population characteristics by ecosystem type for sites at which mean annual figures can be calculated. Based mainly on data in Petersen (69). Respiration has been calculated according to Klekowski et al. (50).

Hourly respiration Mean Mean Wt-specific O~ rate of Nematode Dry individual individual consumption at population abundance weight dry wt fresh wt 20 C (#1)< (#1 O2/m2 Ecosystem Sites (thousands/m2) (rag/m2) (#g) (#g) 10-3/individual/hr) at 20 C)

Tundra I 3,900 180 0.05 0.23 0.50 ] 950 Temperate grassland 6 1,919 +696 217 -----99 0.11 0.57 0.95 1820 (204-3695) Desert 1 423 25 0.06 0.30 0.60 250 Z Evergreen forests 11 2,811 --+620 128 -+25 0.05 0.23 0.50 1410 (911-6954) Deciduous forests 9 1,731 -+563 200 -+115 0.12 0.58 1.0 1730 (178-4430) Tropical forest 1 56 ..... ~,..°

°°

U, 216 Journal of Nematology, Volume 11, No. , July 1979 tylenchus was dominant at the two driest at which neither soil moisture nor soil tem- sites but at the next site was mixed with perature is limiting during the year. On an Macroposthonia, which occurred at all the annual basis, plant herbage yield was re- wetter sites; RadophoIus occurred at the lated more closely to nematode numbers wettest site and Pratylenehus at the preced- than to soil phosphorus or percent soil ing site. There was a high correlation organic carbon (118). Assessment of root (0.89***) between total nematodes and production would be useful in such situa- Truog P, a measure of readily available soil tions; the relations between root production phosphorus, and a lesser correlation (0.69t) and soil biota have been discussed by Cole- with percent soil organic carbon; both of man (15). these relate to plant ga'owth in an area Wasilewska (97) reported on nematodes where phosphorus availability limits plant in six afforested dunes ill Poland; four growth, and it is to this that the nematode formed an establishment succession over populations are causally correlated. 6-20 years, and the other two were 135-yr- In a series of 11 grazed Lolium perenne/ old forests of differing composition. Nema- Trifolium repens pastures the vertical dis- tode abundance, biomass, and metabolism tribution of total nematodes in 0-30 cm soil had a strong positive correlation with soil had an overall correlation of 0.95*** with humus content and tile degree of vascular Truog P and of 0.89*** with percent soil plant cover, particularly in the early (and organic carbon (118). Fig. 1 shows the presumably more productive) stages of the relationship between annual mean total succession. Tile contribution of fungivores to numbers and biomass increased with 20 time. The overall mean individual weight z ol decreased through the succession, although most markedly in plant-feeding nematodes, corresponding to a shift from 60%~ plant- o2 feeding nematodes at 6 yr to 15% at 17-20 e5 years. Fungivores and plant feeders had

o6 maximum numbers in the spring, bacterial rn'~3 ~2 feeders maintained relatively large numbers ~ r33 o7 .T.-~ and biomass throughout the year, and omnivores, fungivores, and plant feeders were reduced in winter. Omnivores and hacterial feeders made the greatest contribution to oxygen consumption.

0 I I I I I Nielsen (63) sampled a 25-m beach 0 1 2 3 4 r~ transect and found a fourfold population MEAN MONTHLY TOTAL NEMATODE5 increase to the seaward end, where there (millions /m 2 m D-10cm soil was a significant contribution by marine species. Sampling slopes FIG. 1. Relationship between mean monthly Corynephorus total nematode populations and pastnre herbage showed a gradation in abundance and production at nine New Zealand pasture sites. Soil diversity from bare areas (175,000/m2; 10 types on which the sites were situated are: 1, Levin; spp) to under Ononis (1,200,000/m2; 18 2, Otiake with irrigation; 3, Rotoiti; 4, Tokomaru spp). Nielsen correlated tile degree of vege- with irrigation; 5, Tokomarn dryland; 6, Kokotau; 7, Judgeford; 8, Pomare; 9, Otiake dryland. The re- tative cover with nematode density. gression equation for sites 2-9 is y = 44.5 + 7.89x; Relation between nematodes and pri- the regression coefficient is significant at 0.001%. See mary production of ecosystems: Primary text for further information (118). production is the biomass which is incor- nematode population estimates and annual porated into a plant community during a herbage dry-matter production for nine specified period; normally respiration losses grazed New Zealand pastures over a wide are ignored and net production given, and range of soil types and conditions. There is often only the above ground portion is a significant linear regression of herbage assessed. Nielsen (63) considered total production on nematode population density nematode populations and suggested that at eight sites; the ninth aberrant site is one nematode abundance is linked with lux- Nematodes in Ecosystems: Yeates 217 uriant vegetation cover (i.e., greater primary TABLE 2. Influence of stocking rate (sheep/ha) production), while Stockli (87) suggested a on nematode abundance in 0-25 cm soil, and standing pasture in Australian Phalaris/Tri[olium pas- link with readily decomposing organic sub- tures. After King et al. (48). strate. Andrews et al. (3) reported that in a shortgrass prairie ecosystem "Grazing by Mean cattle has a minor effect on primary produc- nematodes Green Dead Washed tion. It contrast, it is postulated that grazing /m~ herbage herbage roots by invertebrates, such as plant-parasitic Sheep/ha (1,000s) (kg din/ha) nematodes, may have a major impact on primary production" (seasonally limited 10 270 3125 4225 6800 nematode activity has since been reported 20 191 1959 1238 4263 for the prairie (79) but does not basically 30 101 620 104 2516 alter relationships). Some of these relationships can be demonstrated experimentally total nematode abundance [663,000 cf [e.g., multiplication of Panagrolaimus 344,000/m 2 in 0-I0 cm soil depth (118)]. rigidus reflects the amount of decaying From a grazing trial at that site, Yeates organic material (53)], but the overall (114) reported that an increase in stocking picture can be obtained only from compara- rate, liming, and phosphate fertilizer sig- tive studies of ecosystems. This section nificantly increased total numbers of consitlers total nematode populations in nematodes and of certain components (e.g., relation to environment. Preference is given Pratylenchus, Mononchidae). This result is to mean annual figures hased on monthly or similar to that from Armidale, where pas- quarterly sampling, although some data ture herbage production was greater (12,300, ttsed are less-well based. vs. 12,000 kg DM/ha/yr) in tile year when Environmental management commonly there were significantly more nematodes leads to changes in plant productivity and from tile highly stocked area (1,950,000/m 2 in total and specific nematode populations. at 22.2 sheep/ha, vs. 1,610,000/m 2 at 14.8 Relationships hetween nematode popula- sheep/ha). tion size, rate of multiplication, and the Preliminary results from a study in growth of host plants have been reviewed which Pinus radiata seedlings were planted (8, ,t5), but those relate primarily to plant- at a range of densities in pasture, and feeding nematodes in agricultural systems, grazing continued, also indicate a clear including their interaction with climatic relation between decreased pasture herbage stress. However, comparisons of manage- production and decreased total nematode ment regimes differing in intensity, or the abundance in 0-10 cm soil in plots contain- replacement of one ecosystem by another, ing more trees/ha (118). can give useful information on the com- Cattle grazing for 28 years at the Cotton- ponents of the nematode fauna. That is wood grassland site in South Dakota was particularly true when the hematology is on correlated with a decrease in biomass of a strictly comparable basis. plant-feeding nematodes due to the absence In a Phalaris tuberosa/Trilolium repens of Xiphinema americanum, the largest spe- pasture at Armidale, Australia, nematode cies at the ungrazed site, a slight decrease in abundance decreased in a strong correlation total nematode biomass, and a slight up- with decreased plant herbage and roots ward displacement of vertical distribution whett stocking rates with sheep were higher patterns with vegetation changes which (Table 2) (48). Although only total nema- apparently led to a general increase in tode abundance was assessed, the smaller Tylenchorhynchus spp. (78). Treating the root weights and litter production at the grazed site with Vydate reduced nematode higher stocking rates would clearly reduce populations by 52-82% and increased food available to plant- and bacterial- herbage yield by 28-59%; with the domi- feeding nematodes. Results were similar for nance of plant-feeding nematodes (69% of two adjacent mowing trials at Masterton, numbers; 40-45% of biomass) it appears New Zealand, where the significant differ- they may limit productivity. Smolik (78) ence in cumulative pasture herbage yield used a relationship between nematode bio- (16,900 cf 9,800 kg D.M./ha) is reflected in mass, respiration, assimilation efficiency, 218 Journal of Nematology, Volume 11, No. 3, July 1979 and activity to calculate the net food intake production increase may reflect the input by nematodes, and found they consumed of readily available nutrients, the great more than grazing cattle (Table 3). Sub- increase in ammonifying bacteria (18), and sequent work (79) suggests the nematodes the decomposition processes that may occur were active only from June to September, in manure on the surface of soil, where not April to October as assttmed in calculat- nematodes were not assessed (47). Un- ing Table 3; this is a reduction to 4/7, fortunately, the factors normally limiting which would reduce nematode intake to pasture production are not specified, and about 22 and 32 g/m 2, which is still com- the methods of assessing herbage production parable to intake by cattle. A similiar may lead to significantly different annual adjustment should also be applied to production estimates. There may also be a Smolik's results as used in assessing the significant difference in nematode feeding importance of nematodes in ecosystems (3, habits, in that the (unassessed) natural 16), but that affects the conclusions only manure microbivores increased in Poland slightly. whereas in New Zealand there was a marked The Cottonwood study showed the ef- increase in plant-feeding Prat),lenchus. fects of 28 years of grazing. In a shrub-steppe In a Polish Arrhenatheretum pasture ecosystem in Washington (81), 3 years of receiving two rates of NPK fertilizer in grazing and natural fire were not found to three successive years, there were no signif- influence nematode abundance or biomass. icant changes in abundance, biomass, or The lack of change may be due to the initial metabolic activity of nematodes (100). Urea absence of the large Xiphinema ameri- as tile nitrogen source may have bypassed canum, or the time elapsed since treatment some steps of the normal nutrient cycle, as may have been insufficient for population is suggested by the failure to increase root changes to become significant. biomass (72) despite a fourfold increase in Wasilewska (98, 99) studied a moun- hay yield (90). tainous Polish pasture. Although the In a Swedish Scots pine (Pinus silvestris) penning-up of sheep increased annual pas- plantation with a herb layer including ture production from 200 g/m 2 to 396 g/m 2 Calluna, Vaccinium, and lichens, the best (18), there was a depression in annual relation between nematode abundance and nematode abundance and its estimated plant weight was a negative association metabolism. In ungrazed pasture, total between Tylenchus spp. and the below- nematode abundance and metabolism de- ground standing crop of Calluna vuIgaris. creased with increase in the intensity of There was a positive relation between num- fertilizing with sheep manure. Analysis by bers of root- and fungal-feeding nematodes feeding groups, however, shows some in- and biomass of fine roots of P. silvestris and crease in bacterial feeders, fungivores, and Vaccinium vitis-idaea. These results suggest plant-feeding nematodes with increased that Pinus and Vaccinium or their mycor- manure, while omnivores and predators de- rhizae are food sources for Tylenchus. Slight creased greatly. That differs from results in correlations may be due to sampling tech- Australia and New Zealand. While the nique, to non-limiting food resources, or to difference may be due to a single event the problem of partitioning the nematode rather than sustained management, the food supply between fungi and plant roots TABLE 3. Estimated annual intake of primary (83). production by cattle and nematodes at the Cotton- In five American deserts the rate of wood grassland site, South Dakota, U.S.A.; their nematode population decrease below and biomass is also given; all measurements are dry weights. After Smolik (78). between plants appears to be related to average annual rainfall and plant biomass (i.e., primary production) (30). Intake (g/m2) Biomass(g/m2) The results discussed above indicate a Cattle Nematodes Cattle Nematodes close relationship between herbage and root production in grasslands and between the Ungrazed -- 57 -- 0.54 vertical distribution of nematodes and roots Grazed 22 39 1.69 0.38 in the soil. Annua! production of below- ground matter and the below-ground/ Nematodes in Ecosystems: Yeates 219 above- ground ratios are significantly greater TABLE 4. Correlation between nematode abun- in herbaceous plants than trees, and the dance and number of species for single sampling events in a range of publications. (t denotes p<0.1, absence of significant differences between * p<0.05, ** p<0.01, *** p<0.001). herbs and trees in total dry-matter production shows the importance of including root production in any assessment of productiv- Habitat Sites Correlation Reference ity (13). Half to two-thirds of organic matter in the soil is from dead roots. Under Various 38 + 0.60"** 60 Moss 18 + 0.86" * * 66 grazed pastures, 70% of roots are concen- Soil under 12 +0.81"* 66 trated in the upper 10 cm of soil (90), as are moss the nematodes (116). Under forests, a Dune sand 6 +0.03 105 smaller proportion of plant biomass is Tropical ! 2 + 0.33 112 found in the soil, and although the bulk of soils Tussocks 8 -- 0.16 113 this comprises large roots at considerable Dune sand 10 depths + 0.29 106 depth, small feeder roots and mycorrhizae Festuca 6 depths +0.85* 54 occur near the surface. In forests, nematodes clumps are typically most abundant in tile decomposition zone (F horizon), where there TABLE 5. Mean annual nematode abundance is great microbial activity (92); in mor soils, /m "z and total number of nematode species identified where decomposition takes place above the in different habitats. mineral soil, there are relatively few nematodes in the mineral soil itself. Pastures and Nematodes forests also differ in the origin of their Habitat ]m2 Species Reference litter, and there may be a very rapid cycling of decaying root material (hiring the growth Mixed prairie 6,513,000 80 Smolik (69) of herbs (76). Other ecosystems differ Oak-hornbeam 5,288,000 92 Saly (69) forest similarly. Where vegetation is patchy, nema- (summer) tode population may differ greatly between Beech forest 1.432,000 75 109 vegetational types (55, 85). Such differences Oak forest 1,000,000 22 4 naturally make comparisons of nematode Mixed fen 719,000 13 108 populations between ecosystems difficult Alder-buckthorn 416,000 20 108 carr even when the total metabolic activity of Dune sand 215,000 50 106 the soil is considered. However, again, total Sedge 204,000 17 108 nematode abundance appears positively Buckthorn cart 178,000 12 108 correlated with primary production if one Reed bed 2,400 1 108 avoids agro-ecosystems in which plant- feeding nematodes may be dominant. species) and the range is from more favour- Population density and diversity: Nema- able habitats to less. Within sets of samples tode population diversity has been discussed from similar climate (112) or similar vege- (89, 107) but has not been related to tation (113), other factors influence density population density in soils. Table 4 gives and diversity, and the predominance of such correlations between nematode abundance sets biases the calculation. Arpin (4) found and species diversity for single sampling that the mull soil of a hornbeam (Carpinus events. Values range widely, with no ap- betulus) forest contained more species (30, parent trend. For 34 single-sampling events vs. 22) but fewer total nematodes (255,000, the correlation between abundance and vs. l,O00,O00/m 2) than the acid soil of a diversity is not significant (+0.17). For 10 nearby oak (Quercus sessiliflora) forest. The habitats (Table 5), repeated sampling gives sampling in the hornbeam forest did not a correlation of +0.81"*, and when six cover a full year. other results from limited sampling are in- Volz's (94) data for beech and oak-ash cluded the correlation is + 0.80"**. forest are not strictly comparable with those There are many populations with 10-30 above, being obtained by direct examina- species and densities of 29-8,389 nematodes/ tion of the soil, but indicate 11,903,000 100 g; significant correlations emerge only nematodes/m -° and 26 species in beech when more extreme populations (1-92 forest, compared with 29,815,000/m 2 and 220 Journal of Nematology, Volume 11, No. 3, July 1979 47 species in the oak-ash forest. In arable data are available) and account taken of soils, populations tend to be greater but differing distributions of feeding types with diversity less (25, 88). thne and depth. Assigning nematodes to Trophic structure of nematode popula- feeding groups is difficult because observations: Since Nielsen's (63) work, a series of tions are lacking (88) and specific feeding papers have reported the relative abundance hal)its are diverse. of various trophic gToups of nematodes in a Nematode community structure: Statisti- range of soils; because many omnivores cal analyses of the composition of nematode and predators are large Dorylaimida, this populations by cluster analysis (generally increases their relative contribution to bio- using a 'resemblance equation' or 'three- mass. Vertical distributions of trophic dimensional community ordination', and groups have been reported (6, 86); some showing the relationships in dendrograms) give seasonal changes (86, 98), and some are available for soybean fields, prairies, also consider the influence of extraction streams, and forest woodlots. Studies which method (3l). emphasize the diversity or trophic aspect of The dominance of bacterial feeders in community structure are discussed above. Antarctic mosses, tundra, taiga forests, and In 14 soybean fields, community struc- deserts is noteworthy; in those habitats tures were similar in highly productive dark Angiosperms may be rare and, although soils but in more diverse lighter soils dif- bacterial feeders may start feeding as soon fered between sites and from dark soils (26). as climate permits, other trophic levels may Sampling different habitats in three prairies need to await the development of a food and using the maximum abundance of each chain. In the first four stations in a Pinus species, indicated that variation was greater time sequence on sand studied by Wasilew- between prairie habitats than between ska (97), bacterial feeders tended to increase prairies, and that similar species occur in with age, and that was offset by a decrease similar habitats in all prairies (77). These in omnivores. Nielsen's (63) results can be results express mathematically the commu- recalculated to show similar trends of bac- nity types which were recognised by early terial feeders and omnivores with increasing hematologists as reflecting soil and vegeta- vegetation cover and humus levels. Rever- tion types. sion of Bcoadbalk grassland to wilderness is Sampling of 16 sites in two streams reflected in a change from plant and fungal showed that species presence/absence data feeders to bacterial feeders (119), and re- used in a resemblance equation do not placement of forest by pasture in New relate nematode species to physical condi- Zealand increased plant-feeding nematodes tions at the sites, although community (21). ordination (analysis of quantitative data by In grasslands, ~asilewska (100) found which communities are arranged in multi- that of total nematodes fungivores were dimensional order) did (27). In soybean 3-65% and plant feeders 7-66%. With fields, however, presence/absence data increased stocking (unutilized pasture: (based on a minimum density) gave good pasture: sheepfold) bacterial and plant similarity indices, although the pattern was feeders tended to increase at the expense of somewhat different from that obtained omnivores. Bacterial feeders and omnivores using population densities. When ordina- made the greatest contribution in a grazed tion was based on six predominant species, New Zealand pasture, but under more instead of 154, there was a closer relation- arid conditions plant feeders, particularly ship of these species to the physico-chemical drought-resistant ParatyIenchus, predomi- factors measured. This suggests that these nated (118). six species are the ones influenced most by Although the contribution of various the factors measured and the ones that are feeding types may range from 100% bac- most important in cluster formation: results terial feeders (86) to 93% plant feeders were similar for data from different years. (88), it is clear that there may be definite Future studies might be able to assess the trends along climatic or vegetational gradi- disturl)ance of benthic nematode commu- ents, and it is in the light of those that nities from quantitative data for only a few detailed comparisons should be made (when dominant species (27). Nematodes in Ecosystems: Yeates 221 Nematode communities in 18 Indiana from the previous trophic level, NU is forest woodlots were analysed by several energy not used, C is food ingested, some of methods. Of 175 nematode species, only 18 which is not assimilated but passes as faeces occurred at all sites, but almost 50% oc- (F). The assimilated energy (A) is in- curred at nine of the sites, and similarity corporated in new tissue and reproductive indices gave groupings which reflected plant products (P), used for vital processes, and species associations and soil drainage (41). dissipated as heat; this part of the process, Quantitative ordination analysis gave a normally measured as gaseous exchange, is range from swamp forest communities termed respiration (R). Since assimilation (dominated by Helicotylenchus platyurus) is the part of the matter, or energy, involved to climax oak or beech-sugar maple com- ill metabolism it can be described as the munities (dominated by two Tylenchus spp. energy flow, and few studies of nematodes and Tylenchorhynchus silvaticus), but no have gone beyond estimating this. An intro- clear relationship to edaphic factors was duction to ecological energetics is given in found, although correlations with soil and International Biological Programme Hand- vegetation were better than when similarity books (35, 70), and methods of calculating indices were used (39). Analysis of abun- tile above parameters have been given for dance and live biomass of Tylenchida, enchytraeids (65), Collembola (36), and Dorylaimida, and other nematodes showed annelids and arthropods (68). Although the that Dorylaimida were more diverse but Joule is tile S.I. unit of energy, the calorie less abundant than Tylenchida (40). (1 cal = 4.184 J) is often used in energetics. Dorylaimida were depressed at two 'dis- Respiratory measurements can be con- turbed' sites. Ordination generally reflected verted: 1 ml O2 -- 4.775 cal = 19.979 J for the different communities at the sites, and animals feeding on a mixed substrate. when biomass was used the larger Dory- Some ecologists divide complex systems laimida dominated (40). (defined, however, by habitat boundaries) Analysis of nematodes extracted by into relatively simple units (e.g., species centrifugal flotation from a 16.4-ha area in populations in the ecological sense), whereas Michigan showed that Longidorinae and others divide them into few relatively com- Criconematinae had large 'prominence' and plex units (e.g., trophic levels). Much 'importance' values (52), and detailed ecological information is potentially ap- analysis of 15 criconematid species showed plicable from studies of plant-feeding their overall association with moderately nematodes, but, as regards trophic levels, drained sandy loams under woods, although "creation of correct ecological classification difference between species did occur. of nematodes is a somewhat difficult task These statistical techniques are useful in with the amount of knowledge so far pinpointing key factors influencing nema- available" (97). When specimens are iden- tode communities and have confirmed the tified to genus or species before allocation use of dominant species in assessing changes to a trophic group, more data are available in streams. if the species information appears beside that for trophic groups; that is especially ACTIVITY OF true of Dorylaimida, which have large NEMATODE POPULATIONS individuals but have food habits so poorly Production ecology: Ecological units known that many are regarded as omniv- can be analysed as systems, and the balance ores. measured between a population's intake Laboratory Ieeding studies: Plectus and output of carbon or energy. Three basic parietinus feeding on Acinetobacter sp. equations describe this flow through a ingested 5000 cells per minute, a daily rate biological unit, whether at an individual, of 1.94 × 10-6 g dry weight (dw) or 650% population, or trophic level: of body weight; assimilation efficiency was 12%, while production was 82% of assim- MR = NU + C ilated energy but 10% of consumed energy C =P+R+F (20). Marchant and Nicholas (56) found A =P+R tlle assimilation efficiency of Rhabditis where MR is energy in material removed oxycerca to vary with bacterial concentra- 222 Journal of Nematology, Volume 11, No. 3, July 1979 tion; on average, 37% of ingested food was tam (2). This value was based on mixed respired, 40% defecated, and 22% used in species from field collections dried at 60 C growth. In Caenorhabditis briggsae the and 10 mm Hg; volatiles, which are efficiency of conversion of E. coli was about 11-48% of the dry weight of soil nematodes 13% (61). Feeding in Pelodera chitwoodi (10), are less likely to have been lost than increased endogenous respiration sixfold, from material dried at higher temperatures. and, of energy ingested, juveniles used 27 % In addition to a different fresh-weight as- in respiration and adults 21%; during their sessment, the use of field rather than culture life span females ingested more than three material may also be important; only in times as many bacteria as did males (59). earthworms is attention normally given to P. chitwoodi migrates to and feeds selec- the influence of gut content on dry weights tively on bacteria; resting and dead bacteria (69). did not attract nematodes, and nematode In a hornbeam-oak forest, Saly (75) feeding reduced the proportion of viable found average total nematode biomasses of bacteria in the population (103). 9.615 g/m ~ by Andrassy's method and 4.013 The study of Aphelenchus avenae feed- g/m ~ by drying at 20 C; this suggests a drying on the fungus Botrytis cinerea (84) is matter content of 42 %. complicated by an underestimation of in- There is need for further work on this gestion. Net production efficiency (P/A) subject, including use of interference mi- was 52% in the youngest juveniles, increas- croscopy, but an average dry-matter content ing to 80% in the fourth stage. P/A ratios of 25% can generally be applied. of 6-20% were calculated for A. avenae Calorific value: Known calorific equiv- feeding on Alternaria tenuis (101). How- alents of soil nematodes include 4.284 ever, the lack of a significant influence of cal/mg ashfree substrate for Plectus + initial nematode numbers on fungal growth PoikiIolaimus (110), 5.453 cal/mg dw for suggests that either the populations were Aphelenchus avenae (84), 6.300 cal/mg dw too small to influence fnngal growth or the for Rhabditis oxycerca (56, 62), and 6.316 use of the reduction in fungal weight to cal/mg dw for Caenorhabditis eIegans (62). estimate food intake ignores a significant Those are compatible with values for soil effect of grazing. microarthropods (96) and a wide range of Although these results are similar to animals (34). According to Yeates (110), his results from the field (82, 99, 111, 115), they value is equivalent to 2.152 cal/mg fw. need to be related to environmental fluctua- However, Saly (75) found 9.44 cal/mg, tions and the microcosms discussed below. apparently using the weight of nematodes Dry-matter content: Petersen (69) used dried for 24 h on cotton wool at 20 C. 20% of fresh weight (fw), based on several The calorific value of soil microarthro- published results, which generally involved pods varies seasonally and with feeding direct weighing of nematodes collected from habits (96), and other factors influence the mass cultures, drying at 75-100 C, and re- calorific value of animals (34). Further weighing. Values for Aphelenchus avenae studies are needed on inter- and intraspecific range from 20% (84) to 32% (23), and may variation in calorific values of nematodes. be explicable in terms of the state of hy- Reproductive cycles in the field: The dration, since the moisture contents of reproductive cycles of Heterodera and ApheIenchoides besseyi can range from 5 Meloidogyne have been studied in annual to 80% without 100% mortality (37). crops, but only H. mani and H. trifolii However, nematodes extracted in water have been studied in perennial crops. As- would be expected to be fully hydrated. sessing the reproductive cycles of most other Interference microscopy, using single nema- genera is more difficult because of the dif- todes, generally indicates a dry-matter ficulty in extracting eggs from soil, the content of 25% (67). absence of discrete egg masses, and lack of Yeates (I10) gave a dry weight 58.5% of gross change in body form during ma- the fresh weight, derived from the relation turation. Thorne (88) studied Clarkus biomass = (~¥-~ × L)/(16 × 100,000), where papiUatus, Mylonchulus parab~'achyurus, biomass is in ttg, W is maximum body and M. sigmaturus and concluded that their width, and L is adjusted body length in main period of reproduction was March- Nematodes in Ecosystems: Yeates 223 May, with probably only a single generation J. Phillipson, pers. comm.) (71), while a year. Volz (94) gave sex ratios ranging Sohlenius (82) used carbon-energy budgets from 6 ~ :6 2 for Heterocephalobus elongatus to obtain nematode production of 456 mg to l~:1489 for Plectus cirratus. The oc- C/m'-' (=5.07 kcal/m 2) in a Swedish pine currence of gravid females in 32 species forest. Production in seven California peat- under marram grass has been reported (106), lands was estimated at 0.05-0.20 g wet while seasonal changes in the percentage wt/m~/yr (mean 0.106 g/m 2 -- 0.23 contribution of juveniles, females, and kcal/m 2) (22). males to populations under beech forest Using the amended annual respiration and grazed pastures have been given (111, of 1091 ml O2/m ~ (= 5.21 kcal/m 2) for tlle 117). Various Longidoridae have been stud- Danish beech forest (115) and log P = ied, and the monthly population composi- 0.8262 log R - 0.0948, production is 3.14 tion of Paralongidorus maximus illustrated kcal/m 2, similar to the direct calculation. (12). Analysis of population structure dur- The same equation gives almost un- ing the year indicates periods of recruitment changed production estimates of 17.29-25.29 and mortality. kcal/m 2 for Polish pastures in which juve- Given adequate field population and niles were assumed to have twice the climatic data it should be possible to use respiration rate of adults (98), and 4.57 results from laboratory cultures to interpret kcal/m 2 for the Swedish pine forest. dynamics in the field; Jones's work, partic- ]f Yeates's (111) results are recalculated ularly on cyst-nematodes, shows approaches using monthly changes in total biomass to integration and modelling (43, 46). rather than summing the 29 species, the Laboratory data on Mononchus aquaticus figure obtained is 25% smaller. Species (44) clearly show the influence of tempera- production estimates ranged from 714 /~g ture on the duration of each stage; the basal fw/m2/yr (= 1.54 kcal) for Teratocephalus temperature appears to be 8 C, and up to terrestris to 209,000 pg fw/m2/yr (= 449.8 29 C there is a nearly linear relation be- kcal/m 2) for Aporcelaimus superbus. tween temperature and development. Panagrolaimus rigidus has a temperature Until further estimates of biomass production are made, either directly or using curve similar to that of M. aquaticus (33), fully adjusted respiration rates, no firm although the developmental rate is greater. Reproduction and survival are inter- conclusions can be reached on the pro- related; one stage may better survive adverse ductivity of soil nematode populations, conditions (e.g., eggs in Heterodera cysts, although the 17 available estimates give a second-stage juveniles of Anguina tritici, correlation of 0.69** between mean annual third-stage "dauer" juveniles of Rhabditis, nematode numbers and estimated biomass fourth-stage and adults of Aphelenchoides production. Several approximations have ritzemabosi) (24), but survivorship is rela- been made of total energy ttow through tive and detailed field studies are necessary nematode populations and their estimated efficiency (28, 71, 82, 98, 111). before laboratory results can be used in interpreting population dynamics. Respiration: The respiratory metabo- Nematode biomass production: Several lism of soil nematode populations is found methods have been used to make estimates by multiplying estimated live nematode of nematode production in the field. From biomass by an experimental respiration rate monthly changes in the biomass of 29 spe- over the elapsed time, with adjustment for cies, Yeates (111) calculated an annual field temperature. Information provided by minimum production equivalent to 3.23 Nielsen (63) on respiration of soil nema- kcal/m ~ in a Danish beech forest, while todes has been widely applied (5, 71, 97, Wasilewska used the equation log R = 0.62 110) using a basis figure of 1 ml OJg fw/hr + 0.86 log P to calculate a production of at 16 C, which was adjusted to 0.830 ml 10-12 kcal/m 2 in meadows (100) and 14-25 O2/g fw/hr at 16 C by Yeates (110) to allow kcal/m °- in Polish mountain pastures (98). for biomass calculations with Andrassy The expression log P -- 0.8262 log R - formula (2). 0.0948 (58) gave 1.08 kcal/m ~ in an English Klekowski et al. (50) reviewed data for woodland (correction to published value; 73 species at 20 C and calculated the rela- 224 Journal of Nematology, Volume 11, No. 3, July 1979 tionships R = 1.40 W °.7-" root and shoot production (47). Results have MR = 1.40 W -°.'s attributed to nematodes 0.08-0.21% of the where R is the respiratory rate (t~l x 10-.~/ soil respiration at nine sites on Signy Island ind./hr), W is weight (/,g fw), and MR is (86), 1.94% in an American deciduous the metabolic rate R/W (ttl x 10-3/t~g forest (73), 0.13% in an English beech fw/hr). They found a clear relation between woodland (71), 0.52%, in a Japanese coni- body size and weight-specific respiration ferous forest (49), 1')4 of energy input to a rate. When nematode activity is known (cf. desert soil ecosystem (28), and 0.33% of cryptobiosis, anhydrobiosis, etc.), respiratory the annual carbon input in a Swedish pine calculations should include both weight and forest (82) to nematodes. These results all temperature-specific oxygen consumption, indicate a relatively small role for nema- with the 20 C weight-specific rate being de- todes in soil respiration, which is regarded termined from R = 1.40 W °.z2 and then as similar to carbon cycling in the ecosys- corrected for temperature using Rxo = R20o tem. × q20o/qxo (q values are given by Duncan In agriculture, the great influence on and Klekowski (19)). Sohlenius (82) fol- plant growth of a relatively small plant- lowed such a procedure. nematode biomass is well known, whether Many parameters are usually poorly from direct effects or through increased known, and extensive correction of respira- susceptibility to climatic or nutritional tion, usually derived from non-feeding stress. Twinn (92) used published data (32) specimens in a water drop without soil to calculate that, ignoring turnover, the particles around which to move, may give a production of 15 mg biomass of Rolylenchus false impression of precision. However, a buxophilus led to a 12-g reduction in plant basic temperature correction is normally material. It has been calculated that the loss made. A uniform respiration rate (e.g., 1.52 in pasture production due to the presence ml/g fw/hr at 16 C assuming a mean indi- of 150,000 Heterodera tri[olii cysts/m 2 is vidual biomass of 0.2/~g fw) can be adopted, about 13 times the energy required to pro- or weight-specific rates calculated, whether duce these cysts (118). overall, for each sampling, or for a range of Nematodes have been studied in a wide biomass classes. Other calculations use dif- range of experimental systems, ranging from ferent rates for different feeding groups hanging drops to agar plates, pots, and (from omnivores, 0.7 × 10-~/zl/t~g fw/hr, to microplots. The dynamic interactions of unknown food preferences, 1.5 x 10 -3/~l//~g nematodes with other organisms and nutri- fw/hr at 16 C, without temperature correc- ents have recently been studied using tion) (97) and, following experimental models of portions of natural ecosystems, or results for Panagrolaimus rigidus (51), as- microcosms (1, 74). Just as grazing of suming that juveniles have twice the bacteria by Protozoa (10) and of fungi by respiratory rate of adults (98). Collembola (93) increases nutrient cycling Nematode contribution to ecosystem within the microcosm, so does grazing of metabolism: The International Biological bacteria by amoebae and nematodes. Using Programme placed emphasis on relations a bacterium (Pseudornonas sp.), an amoeba within ecosystems. Respiration was used to (Acanthamoeba sp.), and a nematode assess the contribution of nematodes more (Mesodiplogaster sp.) recovered from the accurately than abundance or biomass fig- rhizosphere of grass, Coleman et al. (17) ures. Problems in estimating respiration studied the effect of these organisms on have been discussed, and results for the processes in microcosms in 50-ml flasks. percentage that nematodes contribute to Their results (Table 6) show that bacterial soil respiration are unadjusted published grazing by nematodes stimulates not only figures. Bunt (14) extrapolated Danish re- respiration but also the net mineralisation sults (63) and calculated 0.5-1.2% for sites of phosphorus and nitrogen (i.e., the avail- on Macquarie Island; and the ]uncus moor ability of plant nutrients). Although, as in results of 0.6-0.7% (5) were adjusted to agronomic pot trials, information obtained 0.2% by Spaull (86) to compensate for from microcosms is valuable, the results are differing sampling depths. In Polish pas- difficult to extrapolate to natural ecosys- tures, nematodes respire 0.29% of plant tems. More work with microcosms is ex- Nematodes in Ecosystems: Yeates 225 TABLE 6. Influence of microbiota on dynamics of experimental microcosms; from results over 0-24 days (17).

Microbiota present Bacteria Bacteria Parameter Bacteria + amoebae + nematodes

CO 2 evolution (#g CO.,-C/g dw) to day 24 1500 1750 1800 % increase in net phosphorus mineralisation to day 17 30 40 73 % nitrogen mineralised to day 17 31 76 81 Extractable ATP (ng ATP/g dw) at day 24 660 360 180 Live bacteria (x 10,/g dw) at day 24 1.9 1.I 0.8 Bacterial biomass (mg/g dw soil) at day 24 0.88 0.20 0.08 petted, and it sltould be supported by field 5. BANAGE, W. B. 1963. The ecological im- studies. portance of free-living nematodes with special reference to those of moorland soil. J. An. Ecol. 32:133-140. CONCLUSIONS 6. BANAGE, W. B. 1966. Nematode distribution ill some British upland moor soils with a note Results for total nematode populations on nematode parasitizing fungi. J. An. Ecol. in lightly managed terrestrial ecosystems 35:349-361. suggest that the populations are correlated 7. BARKER, K. R., C. J. NUSBAUM, and L. A. NELSON. 1969. Seasonal population dynamics with primary production but make only a of selected plant-parasitic nematodes as meas- small contribution to soil respiration. ured by three extraction processes. J. Nematol. Faunas differ greatly in their food sources, 1:232-239. as far as tletermined, and the diversity of 8. BARKER, K. R., and T. H. A. OLTHOF. 1976. feeding habits shows the degree of biological Relationship between nematode population densities and crop responses. Annu. Rev. interaction in the soil. Full understanding Phytopathology 14:327-353. of the role of nematodes in the soil requires 9. BARRETT, J. 1976. Energy metabolism in study, in field and laboratory, of individual nematodes. Pages ll-70 in: The organization genera anti species to obtain data so ttmt of nematodes. N. A. Croll, ed. Academic Press, London. their feeding, respiration, reproduction, and 10. BARSDATE, R. J., R. T. PRENTKI, anti population dynamics can be modelled. T. FENCHEI.. 1974. Phosphorus cycle of Then the effects of their feeding on the food model ecosystems: significance for decomposer sources and on nutrient cycling can be put food chains and effect of bacterial grazers. in perspective. That should help us under- Oikos 25:239-251. l l. BERGE, J. B., A. DALMASSO, and A. KER- stand the complementary roles of plant- MARREC. 1973. Etude des fluctuations des feeding nematodes and those of the detritus populations d'une nematofanne prairiale. Rev. food web in limiting or stimulating plant Ecol. Biol. Sol 10:271-285. growth by making nutrients more readily 12. BOA(;, B., I. E. RASCHKE, and D. J. F. available. BROWN. 1977. Observations on the life cycle and pathogenicity of Paralongidorus maximus in a forest nursery in Scotland. Ann. AppI. LITERATURE CITED Biol. 85:389-397. 13. BRAY, J. R. 1963. Root production and the 1. ANDERSON, R. V., and D. C. COLEMAN. estimation of net productivity. Can. J. Bot. 1977. The use of glass microbeads in ecolog- 41:65-72. ical experiments with bacteriophagic nema- 14. BUNT, J. s. 1954. The soil-inhabiting nematodes. J. Nematol. 9:319-332. todes of Macquarie Island. Austral. J. Zool. 2. ANDRASSY, I. 1956. Die Rauminhalts- und 2:264-274. Gewichtsbestimmung der Fadenwunner 15. COLEMAN, D. C. 1976. A review of root pro- (Nematoden). Acta Zool. Acad. Sci. Hung. duction processes and their influence on soil 2:1-15. biota in terrestrial ecosystems. Symp. Br. Ecol. 3. ANDREWS, R., D. C. COLEMAN, J. E. ELLIS, Soc. 17:417-434. and J. s. SINGH. 1974. Energy flow relation- 16. COLEMAN, D. C., R. ANDREWS, J. E. ELLIS, ships in a shortgrass prairie ecosystem. Proc. and J. s. SINGH. 1976. Energy flow and 1st Int. Congr. Ecology: 22-28. partitioning in selected man-managed and ,t. ARPIN, P. 1975. Etude systematique et dy- natural ecosystems. Agro-Ecosystems 3:45-54. namique de deux nematocenoses en climat 17. COLEMAN, D. C., C. V. COLE, R. V. ANDER- telnpdr6. Rev. Ecol. Biol. Sol 12:493-521. SON, M. BLAHA, M. K. CAMPION, 226 Journal of Nematology, Volume 11, No. 3, July 1979 M. CLARHOLM, E. T. ELLIOTT, H. W. structure in desert soils: nematode recovery. HUNT, B. SHAEFER, and J. SINCLAIR. J. Nematol. 7:343-346. 1977. An analysis of rhizosphere-saprophage 32. GOLDEN, A. M. 1956. Taxonomy of the interactions in terrestrial ecosystems. Ecol. spiral nematodes (Rotylenchus and Helicoty- Bull.-N.F.R. (Statens Naturvetensk Forsk- lenchus), and the development stages and ningsrad) 25:299-309. host-parasite relationships of R. buxophilus 18. CZERWINSKI, Z., H. JAKUBCZYK, n. sp., attacking boxwood. Univ. Md. Agr. A. TATUR, and T. TRACZYK. 1974. Analysis Expt. Sta. Bull. A-85, 28 p. of a sheep pasture ecosystem in the Pieniny 33. GREET, D. N. 1978. The effect of temperature Mountains (the Carpathians). VII. The effect on the life cycle of Panagrolaimus rigidus. of penning-up sheep on soil, microfauna and Nematologica 24:239-242. vegetation. Ekol. Pol. 22:547-558. 34. GRIFFITHS, D. 1977. Caloric content of 19. DUNCAN, A., and R. Z. KLEKOWSKI. 1975. Crustacea and other animals. J. An. Ecol. 46: Parameters of an energy budget. Pages 97-147 593-605, in: Methods for Ecological Bioenergetics. 35. GRODZ1NSKI, W., R. Z. KLEKOWSKI, and W. Grodzinski, R. Z. Klekowski, and A. Dun- A. DUNCAN. 1974. Methods for Ecological can, eds. I.B.P. Handbook 24. Energetics. I.B.t'. Hdbk. No. 24. Blackwell, 20. DUNCAN, A., F. SCHIEMER, and R. Z. Oxford. 367 p. KLEKOWSKI. 1974. A preliminary study of 36. HEALEY, I. N. 1967. The energy ftow through feeding rates ou bacterial food by adult fe- a population of soil Collembola. Pages 695- males of a benthic nematode, Plectus palustris 708 in: ,Secondary Productivity of Terrestrial de Man, 1880. Pol. Arch. Hydrobiol. 21:249- Ecosystems. K. Petrusewicz, ed. Polish Acad. 259. Sci., Warsaw. 37. HUANG, C. S., and S. P. HUANG. 1974. De- 21. EGUNJOBI, O. A. 1971. Soil and litter nema- hydration and the survival of rice white tip todes of some New Zealand forests and pas- nematode, Aphelenchoides besseyi. Nema- tures. N.Z.J. Sci. 14:568-579. tologica 20:9-18. 22. ERMAN, D. C., and N. A. ERMAN. 1975. 38. HUHTA, V., and A. KOSKENNIEMI. 1975. Macroinvertebrate composition and produc- Numbers, biomass and community respiration tion in some Sierra Nevada minerotrophic of soil invertebrates in spruce forests at two peatlands. Ecology 56:591-603. latitudes in Finland. Ann. Zool. Fenn. 12: 23. EVANS, A. A. F. 1970. Mass culture of my- 164-182. cophagous nematodes. J. Nematol. 2:99-100. 39. JOHNSON, S. R., J. M. FERRIS, and V. R. 24. EVANS, A. A. F., and R. N. PERRY. 1976. FERRIS. 1973. Nematode community struc- Survival strategies in nematodes. Pages 383- ture of forest woodlots. II. Ordination of 424 in: The Organization of Nematodes. nematode communities. J. Nematol. 5:95-107. N. A. Croll, ed. Academic Press, New York. 40. JOHNSON, S. R., J. M. FERRIS, and V. R. 25. FERRIS, V. R., and J. M. FERRIS. 1974. Inter- FERRIS. 1974. Nematode community struc- relationships between nematode and plant ture of forest woodlots. III. Ordinations of communities in agricultural ecosystems. Agro- taxonomic groups and biomass. J. Nematol. Ecosystems 1:275-299. 6:118-126. 26. EERR1S, V. R., J. M. FERRIS, R. L. 41. JOHNSON, S. R., V. R. FERRIS, and J. M. BERNARD, and A. H. PROBST. 1971. Com- FERRIS. 1972. Nematode community struc- munity structure of plant-parasitic nematodes ture in forest woodlots. I. Relationships based related to soil types in Illinois and Indiana on similarity coefficients of nematode species. soybean fields. J. Nematol. 3:399-408. J. Nematol. 4:175-183. 27. FERR1S, V. R., J. M. FERRIS, and C. A. 42. JONES, F. G. W. 1973. Management of nema- CALLAHAN. 1972. Nematode community tode populations in Great Britain. Proc. Tall structure: a tool for evaluating water re- Timbers Conf. on Ecological Animal Control source environments. Purdue Univ., Water by habitat Management 4:81-107. Resour. Res. Cent., Tech. Rep. 30, 40 p. 43. JONES, F. G. W, 1975. Accumulated tempera- 28. FRECKMAN, D. W. 1978. Ecology of anhydro- ture and rainfall as measures of nematode biotic nematodes. Pages 345-357 in: Dried development and activity. Nematologica 21: biological systems. Crowe, and Clegg, eds. 62-70. Academic Press, New York. 44. JONES, F. G. W. 1977. Temperature and 29. FRECKMAN, D. W., D. T. KAPLAN, and development of Mononchus aquaticus. Nema- S. D. van GUNDY. 1977. A comparison of tologica 23 : 123-125. techniques of extraction and study of anhy- 45. JONES, F. G. W. 1978. Population dynamics, drobiotic nematodes from dry soils. J. population models and integrated control. Nematol. 9:176-181. Pages 333-361 in: Plant Nematology. 3rd ed. 30. FRECKMAN, D. W., and R. MANKAU. 1977. J. F. Southey, ed. A.D.A.S. Publ. No. GD/1. Distribution and trophic structure of nema- H.M.S.O., London. todes in desert soils. Ecol. BulI.-N.F.R. 46. JONES, E. G. W., R. A. KEMPTON, and J. N. (Statens Naturvensk. Forskningsrad) 25:511- PERRY. 1978. Computer simulation and 514. population models for cyst-nematodes 31. FRECKMAN, D. W., R. MANKAU, and (Heteroderidae: Nematoda). Nematropica 8: H. FERRIS. 1975. Nematode community 36-56. Nematodes in Ecosystems: Yeates 227

47. KAJAK, A. 1975. Energy flow through a moun- of some populations of encbytraeid worms tainous pasture ecosystem. Pages 95-102 in: and treeliving nematodes, Oikos 12:17-35. Progress in Soil Zoology, J. Vanek, ed. Junk, 65. O'CONNOR, F. B. 1963. Oxygen consumption The Hague. and population metabolism of some popula- 48. KING, K. L., and K. J. HUTCHINSON. 1976. tions of Enchytraeidae from north Wales. The effects of sheep stocking intensity on the Pages 32-48 ill: Soil Organisms. J. Doeksen abundance and distribution of mesofauna in and J. van der Drift, Eds. North-Holland, pastures. J. Appl. Ecol. 13:41-55. :~msterdam. 49. K1TAZAWA, Y. 1977. Ecosystem analysis of 66, OVERGAARD (NIELSEN), C. 1948. Studies the subalpine coniferous forest of the Shi- on the soil microfauna. I. The moss inhabit- gayama IBP area, central Japan. Japanese ing nematodes and rotifcrs. Publ. Soc. Sci. I,B.P. Synthesis, Tokyo. 199 p. Lettr. d'Aarhus, Ser. Sci. Nat. 1:1-98. 50. KLEKOWSKI, R. Z., L. WASILEWSKA, and 67. PERRY, R. N. 1977. A reassessment of the E. PAPLINSKA. 1972. Oxygen consumption variations in the water content of the larvae by soil-inhabiting nematodes. Nematologica of Nematodirus battus during the hatching 18:391-403. process. Parasitology 74:133-137. 51. KLEKOWSKI. R. Z., L. WASILEWSKA, and 68. PERSSON, T., and U. LOHM. Energetical E. PAPLINSKA. 1974. Oxygen consumption significance of the annelids and arthropods in in the developmental stages of Panagrolaimus a Swedish grassland soil. Ecol. BulI,-N.F.R. rigidus. Nematologica 20:61-68. (Statens Naturvetensk. Forskningsrad) 23:1- 52. KNOBLOCH, N., and G. W. BIRD. 1978. 211. Criconematinae habitats and Lobocriconema 69. PETERSEN, H. in press, Composition, density thornei n. sp. (Criconematidae: Nematoda). and biomass of the soil fauna. In: Decomposi- J. Nematol. 10:61-70. tion and Soil Processes. D. Parkinson, ed. 53. KOZLOWSKA, J., and K. DOMURAT. 1971. International Biological Programme. Cam- Research on the biology and ecology of bridge University Press. Panagrolaimus rigidus (Schneider) Thorne. 70. PETRUSEWICZ, K., and A. MACFADYEN. IlI, Plant influence on the development of 1970. Productivity of Terrestrial Animals. P. rigidus populations. Ekol. Pol. 19:723-726. I.B.P. Hdbk No. 13. Blackwell, Oxford, 190 p. 54. KRNJAIC, D., and S. KRNJAIC. 1976. Distri- 71. PHILLII'SON, J., R. ABEL, J. STEEL, and bution of nematodes in clumps of Festuea S. R. J. WOODELL. 1977. Nematode num- vaginata. Nematol. Meditera~. 4:161-170. bers, biomass and respiratory metabolism in 55. KUZMIN, L, L. 1976. Free-living nematodes in a beech woodland--Wytham Woods, Oxford. the tundra of western Taimyr. Oikos 27:501- Oecologia (Bed.) 27:141-155. 505. 72. I'LEWCZYNSKA-KURAS, U. 1976. The effect 56. MARCHANT, R.. and W. L. NICHOLAS. of intensive fertilization on the structure and 1974. An energy budget for the free-living productivity of meadow ecosystems. 7, Esti- nematode Pelodera (Rhabditidae). Oecologia mation of biomass of the underground parts (Bed.) 16:237-252. of meadow herbage in the three variants of 57. MARSHALL, V. G. 1977. Effects of manures fertilization. Pol. Ecol. Stud. 2:63-74. and fertilizers on soil fauna: a review. 73. REICHI,E, D. E. 1977. The role of soil in- Commonw. Bur. Soils, Harpenden, Spec. Publ. vertebrates in nutrient cycling. Ecol. Bull.- 3.79p. N.F.R. (Slatens Naturvetensk. Forskningsrad) 58. McNEILL, S., and J. H. LAWTON. 1970. An- 25:145-156. nual production and respiration in animal 74. ROSSWALL, T., U. LOHM, and B. SOH- populations, Nature (Lond.) 225:472-474. LEN1US. 1977. Developpement d'un mi- 59. MERCER, E. K., and E. J. CAIRNS. 1974. crocosme pour l'6tnde de la mineralisation et Food consumption of the free-living aquatic de l'absorption radiculaire de l'azote dans nematode Pelodera chitwoodi. J. Nematol. l'humus d'une for6t de confreres (Pinus 5:201-208. sylvestris L.). Lejeunia 84:1-24. 60. MICOLETZKY, H. 1925. Die freilebenden 75. SALY, A. 1975. [Study of biomass and calorific Susswasser- und Moornematoden Danemarks. value of the soil nematode population in K. Dan. Vidensk. Selsk. Biol. Skr., ser. 8, 10: hornbeam-oak wood in Bab.] Biologia (Brati- 57-310. slava) 30:615-620. 61. NICHOLAS, W. L., A. GRASSIA, and 76. SAUERBECK, D. R., and B. G. JOHNEN. S. VISWANATHAN. 1974. The efficiency 1977. Root formation and decomposition dur- with which Caenorhabditis briggsae (Rhab- ing plant growth. Pages 141-148 in: Soil ditidae) feeds on the bacterium, Escherichia Organic Matter Studies. Vol. 1. Int. Atomic coli, Nematologica 19:411-420. Energy Agency, Vienna. 425 p. 62. NICHOLAS, W. L., and A. C. STEWART. 77. SCHMITT, D. P., and D. C. NORTON. 1972. 1978. The calorific value of Caenorhabditis Relationship of plant parasitic nematodes to elegans (Rhabditidae). Nematologica 24:45-50. sites in native Iowa prairies. J. Nematol. 4: 63. N1ELSEN, C. O. 1949. Studies on the soil 200-206. microfauna. II. The soil inhabiting nema- 78. SMOLIK, J. D. 1974. Nematode studies at the todes. Nat. Jutlandica 2:1-131. ('ottonwood site. U.S.-I,B.P. Grassland Biome 64. NIELSEN, C. O. 1961. Respiratory metabolism Tech. Kept. 251. Fort Collins, Colorado. 80 p. 228 Journal o[ Nematology, Volume 11, No. 3, July 1979

79. SMOLIK, J. D. 1975. Effect of soil temperature 95. WALLACE, H. R. 1973. Nematode Ecology and soil water on reproduction of nematode and Plant Disease. Edward Arnold, London. populations indigenous to the Cottonwood 228 p. site. U.S.-I.B.P. Grassland Biome Tech. Rept. 96. WALLWORK, J. A. 1975. Calorimetric studies 292. I;ort Collins, Colorado. 25 p. on soil invertebrates and their ecological 80. SMOLIK, J. D. 1978. Influence of previous significance. Pages 231-240 in: Progress in insecticidal use on ability of carbofuran to Soil Zoology. J. Vanek, ed. Junk, The Hague. control nematode populations in corn and 97. WASILEWSKA, L. 1971. Nematodes of the effect on corn yield. Plant Dis. Rep. 62:95-99. dunes in the Kampinos forest. II. Community 81. SMOLIK, J. D., and L. E. ROGERS. 1976. structure based on number of individuals, Effects of cattle grazing and wildfire on soil state of biomass and respiratory metabolism. dwelling nematodes of the shrub-steppe eco- Ekol. Pol. 19:651-688. system. J. Range Management 29:304-306. 98. WASILEWSKA, L. 1974. Analysis of a sheep 82. SOHLENIUS, B. in press. A carbon budget for pasture ecosystem in the Pieniny Mountains nematodes, rotifers and tardigrades in a (The Carpathians). XIII. Quantitative distri- Swedish coniferous forest soil. Holarctic bution, respiratory metabolism and some Ecology. suggestion on production of nematodes. Ekol. 83. SOHLENIUS, B., H. PERSSON and C. MAG- Pol. 29:651-668. NUSSON. 1977. Distribution of roots and 99. WASILEWSKA, L. 1975. Quantitative distri- nematodes in a young scots pine stand in bution and respiratory metabolisms with central Sweden. Ecol. Bull.-N.F.R. (Statens suggestions on production of nematodes on Naturvetensk. Forskningsrad) 25:340-347. mountain pastures. Pages 133-140 in: Progress 84. SOYZA, K. 1973. Energetics of Aphelenchus in Soil Zoology. J. Vanek, ed, Junk, The avenae in nmno-axenic culture. Proc. Hague. Hehninth. Soc. Wash. 40:1-10. 100. WASILE'~VSKA, L. 1976. The effect of intensive 85. SPAULL, V. W. 1973. Qualitative and quanti- fertilization on the structure and productivity tative distribution of soil nematodes of Signy of meadow ecosystems. 13. The role of nema- Island, South Orkney Islands. Br. Antarct. todes in the ecosystem of a meadow in Surv. Bull., Nos. 33 8c 34:177-184. Warsaw environs. Pol. Ecol. Stud. 2:137-156. 86. SPAULL, V. W. 1973. Distribution of nematode 101. WASILEWSKA, L.. H. JAKUBCZYK, and feeding groups at Signy Island, South Orkney E. PAPLINSKA. 1975. Production of Islands, with an estimate of their biomass and Aphelenchus avenae Bastian (Nematoda) and oxygen consumption. Br. Amarct. Surv. Bull., reduction of mycelium of saprophytic fungi No. 37:21-32. by them. Pol. Ecol. Stud. 1:61-73. 87. STOCKLI, A. 1952. Studien uber Boden- 102. WASILEWSKA, L. and E. PAPLINSKA. 1976. nematoden mit besonderer Berucksichtigung Methods of soil sampling and estimation of des Nematodengehahes yon Wald-, Grunland- numbers, biomass and community structure und ackerbaulich genotzten Boden. Z. Pflan- of soil nematodes. Ekol. Pol. 24:593-606. zenernaehr Dueng Bodenkd 59:97-139. 103. WASILEWSKA, L., and J. M. WEBSTER. 1975. 88. THORNE, G. 1927. The life history, habits Free-living nematodes as disease factors of and economic importance of some mononchs. man and his crops. Int. J. Environ. Stud. 7: J. Agr. Res. (Wash.) 34:265-286. 201-204. 89. TIETJEN, J. H. 1976. Distribution and species 104. WILT, G. R., M. M. JOSHI, and J. METCALF. diversity of deep-sea nematodes off North 1973. Studies on the interactions of bacteria Carolina. Deep-Sea Res. 23:755-768. and nematodes. Water Resourc. Res. Inst., 90. TRACZYK, T., H. TRACZYK, and D. PAS- Anburn Univ., Alabama. Btdl. 10. 89 p. TERNAK. 1976. The effect of intensive fer- 105. YEATES, G. W. 1967. Studies on nematodes tilization on the structure and productivity of from dune sands. 9. Quantitative comparison meadow ecosystems. 4. The influence of in- of the nematode faunas of six localities. tensive mineral fertilization on the yiehl and N.Z.J.Sci. 10:927-948. floral composition of meadows. Pol. Ecol. 106. YEATES, G. W. 1968. An analysis of annual Stud. 2:39-47. variation of the nematode fauna in dune sand 91. TROUGHTON, A. 1957. The underground at Himatangi Beach, New Zealand. Pedobio- organs of herbage grasses. Commonw. Bur. logia 8:173-207. Past. & Field Crops, Bull. 44. 163 p. 107. YEATES, G. W. 1970. The diversity of soil 92. TW1NN, D. C. 1974. Nematodes. Pages 421-465 nematode faunas. Pedobiologia 10:104-107. in: Biology of Plant Litter Decomposition. 108. YEATES, G. W. 1971. Plant and soil nematodes C. H. Dickinson and G. J. F. Pugh, eds. Vol. of Wicken Fen. Nat. Cambs. 14:23-35. 2. Academic Press, London. 109. YEATES, G. W. 1971. Feeding types and feed- 93. van der DRIFT, J., and E. JANSEN. 1977. ing groups in plant and soil nematodes. (;razing of springtails on hyphal mats and Pedobiologia 11 : 173-179. its influence on hyphal growth and respira- 110. YEATES, G. W. 1972. Nematoda of a Danish tion. Ecol. Bull.-N.F.R. (Statens Naturvetensk. beech forest. I. Methods and general analysis. Forskuingsrad) 25:203-209. Oikos 23:178-189. 94. VOLZ, P. 1951. Untersuchungen uber die 111. YEATES, G. W. 1973. Nematoda of a Danish Microfauna des Waldbodens. Zool. Jahrb. beech forest. II. Production estimates. Oikos Abt. Syst. Oekol. Geogr. Tiere 79:514-566. 24:179-185. Nematodes in Ecosystems: Yeates 229

112. YEATES, G. W. 1973. Abundance and distribu- 116. YEATES, G. W. 1977. Soil nematodes of New tion of soil nematodes in samples from the Zealand pastures. Soil Science 123:415-422. New Hebrides. N. Z. J. Sci. 16:727-736. 117. YEATES, G. W. 1978. Populations of nematode 113. YEATES, G. W. 1974. Studies on a climose- genera in soils under pasture. II. Seasonal quence of soils in tussock-grassland. 2. dynamics in dryland and elfluent irrigated Nematodes. N.Z.J. Zool. 1:171-177. pastures on a central yellow-grey earth. N. Z. 114. YEATES, G. W. 1976. Effect of fertilizer treat- J. Agr. Res. 21:331-340. ment and stocking rate on pasture nematode 118. YEATES, G. W. Unpublished results. populations in a yellow-grey earth. N. Z. J. 119. YUEN, P. H. 1966. The nematode fauna of the Agr. Res. 19:405-408. regenerated woodland and grassland of 115. YEATES, G. W. 1977. Nematoda of a Danish Broadbalk Wilderness. Nentatologica 12:195- beech forest--a correction. Oikos 28:309. 214.

Influence of Temperature on Population Development of Eight Species of Pratylenchus on Soybeaff

NELIA ACOSTA and R. B. MALEK 2 Abstract: In a soil temperature study, population increase on 'Clark 63' soybeatt was most rapid at 30 C in Pratylenchus alleni, P. brachyurus, P. cofleae, P. neglectus, P. scribneri, and P. zeae and at 25 C in P. penetrans and P. vulnus. The last two were the only species that reproduced at 15 C. Populations of all species increased over the range of 20-30 C, except those of P. neglectus at 20 C and P. coffeae, which was not tested below 25 C. Only P. brachyurus, P. neglectus, P. scribneri and P. zeae reproduced at 35 C. At their optimum temperatures, P. scribneri exhibited the greatest population increase, 1248-fold, and P. penetrans the least, 32-fi~ld. This is the first report of soybean as a host for P. vulnus. Key Words: Pratylenchus alleni, P. brachyurus, P. cofleae, P. neglectus, P. penetrans, P. scribneri, P. wtlnus, P. zeae, lesion nematodes, host-parasite relationships, ecology, susceptibility, Glycine max.

The activity of soil-inhabiting nema- Pratylenchus brachyurus (Godfi'ey) Filipv. todes is influenced to some degree by each and Schuurm.-Stekh. populations in roots of the many biotic and abiotic factors iu of several cultivars generally increased with their complex environment. Temperature is temperature up to the test maximum of particularly important, affecting movement, 29 C. rate of growth and reproduction, sex de- Greenhouse culture tests have indicated termination, relative abundance of food, that several species of Pratylenchus repro- and expression of nematode damage to duce rapidly on soybean during the summer plants (11). There have been numerous re- months. This study was conducted to deter- ports concerning the influence of this factor mine the influence of temperature on the on host-nematode relationships but few in- population development on soybean of P. volving soybean (Glycine max [L.] Merr.) alleni Ferris, P. brachyurus, P. coffeae and lesion nematodes. Knowledge of the (Zimmerman) Filipv. and Schuurm.-Stekh., effects of temperature on population de- P. neglect~ls (Rensch.) Filipv. and Schuurm.- velopment of these nematodes on soybean is Stekh., P. penetrans (Cobb) Filipv. and limited to findings of Lindsey and Cairns Schuurm.-Stekh., P. scribneri Steiner, P. (6), who reported that the density of wdnus Allen and Jensen, and P. zeae Graham. Received for publication 11 January 1978. Portion of a Ph.D. dissertation submitted by the senior author to the University of lllinois at Urbana-Champaign. MATERIAL AND METHODS Joint contribution from the Illinois and Puerto Rico Agri- cultural Experiment Stations. Research supported in part Original sources of nematodes were: P. by a fellowship from the Ford Foundation. alleni from Syringa persica L., Onarga, Il- 2 Assistant Nematologist, Department of Crop Protection, University of Puerto Rico, R.U.M. Mayaguez, Puerto Rico linois; P. brachyurus from Ananas comosus 00708. and Associate Professor of Nematology, Department Merr., Corozal, Puerto Rico; P. col~eae from of Plant Patholog3', University of Illinois. Urbana. Illinois 61801. Dioscorea rotundata Poir, Corozal, PR; P.