Oostenbrink, M.

English

Wageningen Yield 

Nematodes in relation to plant growth. II. The 
influence of the crop on the nematode 
population 
M. OOSTENBRINK 
Plant Protection Service / Agricultural University, 
Wageningen, Netherlands 
Summary 
Population studies in three rotation trials demonstrated the marked influence of cropping on nema­
tode populations in cultivated soil. One year's cultivation of different crops caused shifts in the 
population densities of at least four different plant parasitic nematodes in both a silt soil and a 
sandy soil (tables 1 and 3). The influence of one or two years' cultivation of a crop may be 
noticeable in the nematode infestation of subsequent crops for at least two seasons. This appears 
to hold for Heterodera, Meloidogyne as well as for migratory root-infesting species. Table 2 
stresses the decisive influence of one-sided cultures on the appearance of different Heterodera 
species in a field and gives an insight into the epidemiology of Heterodera infestations and the 
preventative value of crop rotation. 
Nine special host-parasite relationships are apparent from the tables and are summarized on 
p. 4 and 5. 
1. Introduction 
The overall occurrence of a dense, mixed population of plant parasitic and saprozoic 
nematodes in cultivated soil was substantiated in publication I of this series (KLEY-
BURG and OOSTENBRINK, 1959). The density of known and suspected plant parasitic 
nematodes from a hundred different fields in the Netherlands ranged from 120 to 
3510, with an average of more than 900 per 100 ml of soil; 77 % of the fields 
contained Heterodera cysts of different kinds. The occurrence of 4—6 genera of plant 
parasites, and also the occurrence of two or more species of a genus at the same 
place appeared to be common. The results of field trials indicated, that the density 
and the composition of a nematode population fluctuate markedly with the crops 
grown. This holds true for the plant parasites, each with its own plant-parasite relation­
ship, and the saprozoic nematodes, which are influenced by the availability of decay­
ing organic matter. Examples have been published earlier (OOSTENBRINK, S' JACOB and 
KUIPER, 1956; OOSTENBRINK, 1957, 1960 a in Druck). In the following tables results 
of three trial fields are recorded to demonstrate the general characteristics of this 
population dynamics. The methods for extracting, counting and analysing of the nema­
todes are described elsewhere (OOSTENBRINK, 1960 b). Some relationships between popu­
lation density of plant parasitic nematodes and the appearance of disease symptoms, 
or rotation effects in subsequent crops, will be reated later. 
Received for publication 18th November, 1960. 
Neth. J. agric. Sei., Vol. 9 (1961) No. 1 (February) 55 
M. OOSTENBRINK 
2. Results 
A. Non-cyst forming nematodes in sandy silt soil at Ellecom 
The original field was fairly uniformly infested in the spring of 1953. The prevailing 
phytophagous genera were Pratylenchus, Tylenchorhynchus and Rotylenchus. Meloido-
gyne, Paratylenchus and some other stylet-bearing genera were present in lower num­
bers, Heterodera was not found here. 
Corn, witloof, potato and beet were each grown on two plots of 100 sq. metres in 
1953. The same crops were grown on the same plots in 1954, except potato which 
was replaced by carrot. In 1955 nine crops were grown on each of the original eight 
plots, increasing the number of plots to 72. The nematode populations were estimated 
TABLE 1. Influence of the last grown and of two preceding crops on a mixed popu­
lation of root-infesting, non-cystforming nematodes in sandy silt soil at 
Ellecom. Four different rotations in 1953—'54. Nine different crops follow­
ing each rotation in 1955. 
Nematode figures determined per 100 ml of soil in the spring of 1956. 
P. == Pratylenchus; T. = Tylenchorhynchus; R. = Rotylenchus; M. = 
Meloidogyne; Pa. = Paratylenchus; O. = other Tylenchida; S. = sapro-
zoic nematodes. 
Nematodes 1956, per 100 ml of soil (mean of eight plots) 
A. Crop 1955 P. T. R. M. Pa. O. S. 
Ley = grass + white clover . . 610 230 410 100 69 200 1100 
Rye (Secale cereale L.) 440 180 290 6 2 240 1030 
Oats (Avena sativa L.) 440 130 290 8 4 260 1180 
Barley (Hordeum vulgare L.) . 420 180 300 4 0 240 990 
Beet (Beta vulgaris L.) 340 43 550 110 6 130 1020 
Potato (Solanum tuberosum L.) 330 32 230 87 0 190 890 
Witloof (Cichorium intybus L.) 260 23 290 14 0 140 1050 
Pea (Pisum sativum L.) 250 71 310 200 0 130 1010 
Carrot (Daucus carota L.) .... 240 31 490 28 0 140 1120 
L.S.D. 1 95 % 128 70 125 67 83 223 
99 % 192 105 188 100 124 335 
F-value 2 7,17++ 10,3++ 5,76++ 8,25++ 3,26+ 1,14— 
Nematodes 1956, per 100 ml of soil (mean of eighteen plots) 
B. Crops 1953 & 1954 P. T. R. M. Pa. O. S. 
Corn — corn 540 220 120 6 4 190 1100 
Witloof — witloof 420 42 410 13 1 170 1040 
Potato — carrot 260 78 420 110 0 220 980 
Beet — beet 240 65 470 120 30 170 1070 
L.S.D. 1 95 % 85 47 84 44 55 149 
99 % 128 70 126 67 83 223 
F-value 2 22,1++ 24,9++ 28,8++ 15,2++ 1,82- 1-
1 As least significant difference at 95 or 99 % level 2y 2 or 3 | 2 times the standard error is 
taken respectively. 
2 Variance ratio. ++ = differences significant at 99 % level, + = at 95 % level, — = non­
significant. 
56 Neth. J. agric. Sei., Vol. 9 (1961) No. 1 (February) 
NEMATODES IN RELATION TO PLANT GROWTH. II 
in soil samples from all 72 plots in the spring of 1956. They are recorded in TABLE 1, 
together with general indications about statistical signifiance of the differences 
observed. 
TABLE 1 A shows, that the population in this field comprises at least five genera 
to which pathogenic species are known to belong. The 1955 crops evidently have 
caused very significant differences in all these genera, as indicated by the F-values 
of the common analysis of variance. The differences in the "other Tylenchida" as 
a whole are barely significant, whereas the "saprozoic nematodes" as a whole do not 
differ in density. 
Further analysis of the differences by means of the "studentized range test" in con­
nection with the analysis of variance (KEULS, 1952) separates the crops listed in 
TABLE 1 into groups according to their efficiency as host plants as follows: 
for Pratylenchus, mainly P. crenatus Loof (indicated earlier as P. pratensis s.l.), the 
crop groups are: ley — rye, oats, barley — the five remaining crops; for Tylencho-
rhynchus, mainly T. dubius (BUETSCHLI): ley — barley, rye, oats — pea — the four 
remaining crops; for Rotylenchus, mainly R. robustus (DE MAN): beet, carrot, ley — 
five other crops — potato; for Meloidogyne, here M. hapla CHITWOOD: pea — beet, 
ley, potato — the five remaining crops. No analysis is made of the Paratylenchus 
figures since too many zero's occurred, however, the range ley — beet — remaining 
crops is suggested. No significant differences were shown to exist by the "studentized 
range test" in the "other Tylenchida" and in the "saprozoic nematodes". 
TABLE 1 B, also based on the nematode figures of spring 1956, shows that the crops 
in 1953 and 1954 are still causing very significant differences (c.f. F.-values) after 
the 1955 crop in all recorded categories of root-infesting nematodes. The "studen­
tized range test" indicates corn as an efficient host plant of Pratylenchus and Tylen-
chorhynchus and as a poor host of Rotylenchus, Meloidogyne and Paratylenchus. 
TABLE 1 B confirms the forementioned data of TABLE 1 A and stresses the indication 
that beet is a good host for Paratylenchus. Only witloof appears as a samewhat 
more efficient host of Pratylenchus than would be expected from TABLE 1 A. 
B. Cyst nematodes in a sandy peat soil at Emmercompascuum 
The field was reclaimed by removing a thick peat layer in 1928 and was therefore 
virgin soil. Three crops of potato, two crops of wheat and one crop of rye were 
grown in the period 1929 through 1934. From 1935 up till the present seven dif­
ferent fixed cropping systems were practised on parallel plots of about 800 sq. metres 
in this field, viz. potatoes every year, potatoes every other year, potatoes every three 
years and monocultures of cereals. From the spring of 1954 on, each plot was 
examined annually for cystforming nematodes. TABLE 2 gives the results obtained 
in 1958; these results did not show real differences from those of other years. 
TABLE 2 demonstrates that three cystforming Heterodera species have reached the 
field, viz. the cereal cyst eelworm H. avenae WOLLENWEBER, the potato cyst eelworm 
H. rostochiensis WOLLENWEBER and the Galeopsis cyst eelworm, H. galeopsidis GOF-
FART. The first-mentioned two species have built up high, in fact noxious, popula­
tions in the plots in which their respective host crops were grown intensively. Plots 
on which potatoes were grown every year and every other year had high nematode 
infestation, whereas no infestation was apparent on fields planted to potatoes every 
third year. Dense populations of H. avenae were apparent on soils planted yearly to 
winter wheat, oats or summer and winter cereals. A dense population of this nema­
tode also occurred in the soil planted to cereals (mainly rye) two times in three 
Neth. J. agric. Set, Vol. 9 (1961) No. 1 (February) 57 
M. OOSTENBRINK 
TABLE 2. Influence of one-sided culture on the appearance of noticeable populations 
of different Heterodera species in a sandy peat soil at Emmercompascuum. 
Seven fixed rotations since 1935. Nematode figures per 40 ml of soil, 
determined in the spring of 1956. 
c. = cysts; vc. = viable cysts; 1. = larvae within cysts. 
Heterodera cysts 
Permanent rostochiensis avenae galeopsidis 
rotational system c. = VC. = 1. c. = vc. = 1. c. = vc. = 1. 
1. Potatoes every year 349 296 = 25640 0 = 0 = 0 0 = 0 = 0  
2. Potatoes every other year 216 — 205 = 30540 3 = 3 = 70 3 = 0 = 0  
(= cereals every other year) 
3. Potatoes every third year 0 — 0 = 0 68 = 5 = 840 2 0 = 0  
(= cereals two times in three years) 
4. Winter rye every year 0 = 0 = 0 150 = 9 = 1480 5 = 5 = 64 
5. Winter wheat every year 0 — 0 = 0 71 = 17 = 1460 8 = 3 = 90 
6. Summer oats every year 0 0 = 0 140 = 14 = 2140 29 = 5 = 90 
7. Summer and winter cereals alterna­
tively 0 0 = 0 33 = 7 = 1000 40 = 1 = 30 
years (= potatoes every third year), but a barely susceptible population was apparent 
in the soil planted to cereals (mainly rye) every other year (= potatoes every other 
year). H. galeopsidis is present in noticeable concentrations in all plots except the 
monoculture potato plot. Host plants of this nematode, Galeopsis and Stellaria spp., 
are associates of the cereal culture here and occur first apparently in the plots on 
which cereals are regularly grown. 
C. Root-infesting nematodes in sandy soil at Alteveer 
The prevailing phytophagous nematodes in this field were Heterodera (mainly avenae), 
Pratylenchus (a mixture of penetrans (COBB) and crenatus), Tylenchorhynchus (mainly 
dubius) and Paratylenchus (an unindentified species). In 1957 four crops, viz. beet, 
oats, potato and rye were grown in long strips. In 1958 the same crops were again 
grown in strips, but at right angles to the 1957 strips. A nematode census was taken 
from all plots in the spring of 1959. The results are recorded in TABLE 3. 
The data from TABLE 3 suggest that the density of all genera has been influenced by 
the crops. Pratylenchus and Tylenchorhynchus seem to be suppressed by beet. Para­
tylenchus, on the contrary, is stimulated markedly by beet. The densest population 
is found on the plot with two years beet in succession (plot nr. 3), however, the 
influence of the beet crop of 1957 is also noticeable on the strips with other crops 
in 1958 (plots nr. 1, 2, 4). Heterodera is strikingly stimulated by rye but not by 
oats. This is visible in the number of free larvae in the soil as well as in the num­
ber of cysts and larvae within cysts. The densest population is found on the mono­
culture rye plot (nr. 14). The influence of the rye crop of 1957 is, as in the case 
with Paratylenchus, also noticeable on the strips with other crops in 1958 (plots 
nr. 13, 15, 16). 
3. Discussion, and conclusion 
TABLE 3 reflects the complexicity of nematode population dynamics on a sandy farm 
soil. The crops are common and the nematodes studied are widespread. It may there-
58 Neth. J. agric. Sei., Vol. 9 (1961) No. 1 (February) 
NEMATODES IN RELATION TO PLANT GROWTH. II 
TABLE 3. Influence of different rotations on a mixed population of root-infesting 
nematodes in sandy soil at Alteveer. Four crops in 1957, the same crops 
in 1958 following all crops of 1957. Nematode figures determined per 100 
ml of soil in the spring of 1959. 
HI. = free Heterodera larvae; Pa. = Paratylenchus; P. — Pratylenchus; 
T. = Tylenchorhynchus; O. = other Tylenchida; S. = saprozoic nematodes, 
c. = cysts; vc. — viable cysts; 1. = larvae within cysts. 
Crops Active nematodes 
Plot 
Nr 1957 1958 HI. Pa. P. T. O. + s. c. = vc. = 1. 
1 Beet Oats 25 230 210 490 4260 38 _ 0 — 0 
5 Oats 55 10 200 545 3960 18 1 = 20 
9 Potato 35 15 410 1045 3850 23 =: 1 — 5 
1: Rye 580 10 165 675 3040 60 = 12 = 290 
695 265 985 2755 15110 139 = 14 315 
2 Beet Rye 210 430 20 495 4115 79 = 26 1150 
6 Oats 315 0 60 1030 3960 36 10 - 360 
10 Potato 265 5 235 620 3140 48 16 — 795 
14 Rye 1190 15 230 1000 4895 145 = 83 = 3340 
1980 450 545 3145 16110 308 = 135 = 5645 
3 Beet Beet 25 3480 45 115 3905 21 = 0 _ 0 
7 Oats 35 10 95 390 2910 26 = 0 = 0 
11 Potato 10 0 15 280 3570 23 = 0 — 0 
15 Rye 325 20 55 175 2905 74 30 = 1070 
395 3510 210 960 13290 144 = 30 = 1070 
4 Beet Potato 160 135 240 585 4075 21 = 4 = 60 
8 Oats 45 25 195 520 4570 17 
= 
1 
= 5 
12 Potato 30 5 115 425 3960 32 = 2 — 55 
16 Rye 445 15 180 610 3775 58 = 16 = 310 
680 180 730 2140 16380 128 23 = 430 
Heterodera avenae cysts 
fore be expected that these population shifts are normally occurring in practice on 
this soil. All four crops differ from each other with respect to one or more phyto­
phagous species. The influence of the lastgrown crop is marked. The Paratylenchus 
and Heterodera figures show, that negligible populations may rise to a high level in 
one or two years. The same figures indicate that the influence on the nematode 
population of one efficient host crop may persist for more years. This was known 
to be true for Heterodera species, but it appears to hold true also for Paratylenchus. 
TABLE 1 illustrates this fact with respect to Pratylenchus crenatus, Tylenchorhynchus 
dubius, Rotylenchus robustus and Meloidogyne hapla. In this experiment the pre­
ceding crops were grown for two years in succession and their influence is therefore 
very distinct. A different cropping history may even decide about the occurrence in 
noticeable numbers of related species as illustrated by TABLE 2. Initial infestations by 
the three Heterodera species recorded can hardly be absent in any of the plots, due 
to extensive distribution by wind and otherwise, but the crops had to bring them to 
Neth. J. agric. Sei., Vol. 9 (1961) No. 1 (February) 59 
NEMATODES IN RELATION TO PLANT GROWTH. II 
the fore. This trial gives an insight into the epidemiology of Heterodera infestations 
and their close association with crop rotation. 
Several special plant-parasite relationships become visible from the tables. Some of 
them are noted earlier, some others will be treated with the help of more data else­
where. Nine cases are listed here as follows without further discussion: 
a. Potatoes every year and every other year caused high populations of Heterodera 
rostochiensis, but potatoes every third year evidently suppressed the nematode up 
till now (TABLE 2). 
b. Monoculture of cereals, including rye, caused high populations of H. avenae. Rye 
every other year evidently kept the nematode at a low level (TABLE 2). 
c. Rye (Petkus) was an efficient host of the H. avenae population at Alteveer, where­
as oats (Marne) was not (TABLE 3). 
d. Weeds in the cereal crops, probably Galeopsis and Stellaria species, built up notice­
able populations of H. galeopsidis (TABLE 2). 
e. Ley, rye, oats, barley and corn were efficient hosts of Tylenchorhynchus dubius 
and of Pratylenchus crenatus (TABLES 1 and 3). 
f. Beet, carrot and ley (probably the white clover component) were efficient hosts 
of Rotylenchus robustus in comparison to potato (TABLE 1). 
g. Pea, beet, ley (white clover) and potato were efficient hosts of Meloidogyne hapla 
(TABLE 1). 
h. Ley and beet were efficient hosts of Paratylenchus sp. (TABLES 1 and 3). 
i. Beet suppressed Pratylenchus, mainly penetrans, in comparison to oats, rye and 
potato (TABLE 3). 
The examples above indicate the behaviour of some of the major species of the 
nematode populations present. More relationships may be present or become evident 
in the same soil. 
ACKNOWLEDGEMENTS 
The author is indebted to Ir. S. H. JUSTESEN and his co-workers of the Centre for 
Mathematics in Agriculture, Wageningen for statistical analysis of the data and to 
Dr. J. KuC of the Purdue University, Lafayette, for his help in preparing the english 
text. 
L I T E R A T U R E  
KEULS, M. 
KLEYBURG, P., and 
M. OOSTENBRINK 
OOSTENBRINK, M., J. J. 
s'JACOB, and K. KUIPER 
OOSTENBRINK, M. 
60 
1952 The use of the "studentized range" in connection with an 
analysis of variance. Euphytica 1, 112—122. 
1959 Nematodes in relation to plant growth. I. The nematode 
distribution pattern of typical farm and nurseries. Neth. J. 
Agric. Sei. 7, 327—343. 
1956 An interpretation of some crop rotation experiences based 
on nematode surveys and population studies. Nematologica 1, 
202—215. 
1957 Das Vorkommen von Artgemischen bei pflanzenparasitären 
Nematoden. Nematologica 2, 342—346. 
1960a Population dynamics in relation to cropping, manuring and 
soil disinfection. Nematology. Ed. J. N. Sasser and W. R. 
Jenkins, Univ. N. Car. Press, Chapel Hill. p. 439—442. 
1960b Estimating nematode populations by means of some selected 
methods. Nematology. Ed. J. N. Sasser and W. R. Jenkins, 
Univ. N. Car. Press, Chapel Hill. p. 85—102. 
(in Druck) Vorfruchtwirkung und Nematoden. 
Neth. J. agric. Sei., Vol. 9 (1961) No. 1 (February) 


Nematodes in relation to plant growth. II. The influence of the crop on the nematode population

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