Bouwman, L.A.

Brussaard, L.

Kools, J.P.

English

Wageningen Yield 

6.7. POPULATION DYNAMICS AND NITROGEN 
MINERALIZATION RATES IN SOIL AS INFLUENCED BY 
BACTERIAL GRAZING NEMATODES AND MITES 1 
L. Brussaard, J.P. Kools, LA. Bouwman and P.C. de Ruiter 
Institute for Soil Fertility, P.O. Bo* 30003, 9750 RA Haren, The Netherlands 
INTRODUCTION 
The work presented in this paper is part of the Dutch Programme on Soil Ecology of Arable 
Farming Systems (Brussaard et al., 1988). This programme includes a comparison of the 
functioning of the soil/plant ecosystems of high and reduced input arable farming at the 
Lovinkhoeve experimental farm. This farm is located on a calcareous sandy loam soil in 
the Noordoostpolder, which was reclaimed from Lake Yssel in 1942. In our case reduced 
input means a smaller nitrogen addition and a larger proportion of nitrogen added as manure. 
The use of organic manure might contribute to a solution for the great manure surpluses 
in the Netherlands. In organic-nutrient, input farming the crop is more dependent on the 
activity of soil organisms for its supply with nutrients. Appropriate management of the 
soil biota may help to improve the efficiency of nutrient use in agroecosysterns (Elliott 
and Coleman, 1988). Therefore, knowledge of the relation between population dynamics 
in the soil ecosystem and the rate of nitrogen mineralization is required. 
We carried out a microcosm experiment in which we studied the population dynamics 
of bacteria, protozoa, nematodes and mites and the effects of these organisms on nitrogen 
mineralization. The experiment comprised four series: bacteria with protozoa, bacteria with 
protozoa and nematodes, bacteria with protozoa and mites and bacteria with protozoa, 
nematodes and mites. We used the nematode Acrobeloides bâtschli and the mite Histiostoma 
litorale, both of which are assumed to feed on bacteria only. So we had possible competition 
for bacteria among amoebae, flagellates, nematodes and mites. Protozoa and nematodes, 
both separately and in combination, have been shown to affect the population dynamics 
of bacteria and to stimulate the nitrogen mineralization in microcosms (Clarholm, 1981; 
Coleman et al., 1977; Coleman et ai, 1983). Mites and springtails generally accelerate 
the decomposition of litter but they stimulate the mineralization of nitrogen in only half 
of the cases reviewed by Seastedt (1984). Predatory mites may reduce the number of 
1 Communication no. 6 of the Dutch Programme on Soil Ecology of Arable Farming Systems. 
517 
518 Management and Conservation of Soil Fauna 
bacteriovorous nematodes so that the latter do not overgraze the microflora to such an extent 
that the mineralization of nitrogen is retarded (Santos et al., 1981; Elkins and Whitford, 
1982) but this effect is not always apparent (Parker et al., 1984). However, we are not 
aware of any studies concerning bacteriovorous mites. 
The objective of the present study was to assess the influence of possible competitors 
at the grazer's trophic level on the numbers of bacteria as well as bacterial grazers and 
on the concomitant nitrogen mineralization. 
MATERIAL AND METHODS 
We filled 72 glass pots of 1 1, four series of 18 pots each, with 600 g (dry weight) of 
a calcareous sandy loam soil (pH-KCL 7.3; organic matter content 2.4%; mineral nitrogen 
content 12 mg/kg), to which 1 g lucerne meal was added, i.e., 60 mg N per kg soil. The 
soil was sterilized by y-radiation (2.5 MRad) after drying at 5°C to 30% WHC and passed 
twice through a 8 mm sieve. 
One series of pots was inoculated with a soil suspension with bacteria and protozoa 
(amoebae and flagellates); this was the BP-treatment. Bacteria and protozoa were collected 
by filtering a suspension of the soil through a 25 (im filter. The soil from which the 
suspension was made came from the same site as that added to the pots and had been heat-
treated (24 hours at 50°C, two days at room temperature, 12 hours at 50°C) to kill nematode 
eggs that might have passed the filter. The second series received this suspension plus the 
nematode species Acrobeloides bâtschli (BPN-treatment). Acroheloides bâtschli was cultured 
in soil (heat-treated as described above), to which lucerne meal and a non-heat-treated soil 
suspension, filtered through a 1.5 (im filter, had been added. The nematodes were eluted 
with sterile water and added in suspension to the pots (approximately 2000 per pot, i.e. 
approximately 3 per g soil). The third series received the heat-treated suspension plus the 
mite species Histiostoma litorale (BPH) and the fourth the suspension plus nematodes and 
mites (BPNH). Histiostoma litorale is an anoetid mite measuring 400-500 (im in length 
(deutonymph to adult). It has chelicerae transformed to combs that cause a water current 
from which bacteria are filtered under moist conditions (Woodring, 1963). The mites were 
cultured on agar plates (15% agar + some glycine) and 25 individuals were added per pot, 
i.e., approximately 4 per 100 g soil. Both A. biitschli and H. litorale are bacteriovorous 
and among the most abundant species captured in the soil of our experimental fields. The 
moisture content of the soil in the pots was adjusted to 24% (w/w). The bulk density was 
1.39 x 103 kg m'\ 
The pots were incubated at a light/dark and temperature regime comparable with that 
in the field in spring (L/D: 14/10); the temperature was set at 14°C during the day and 9°C 
during the night. We found that under these conditions the life cycle of the mite is 2-2.5 
weeks. The pots of each series were analysed after 1, 2, 3, 6, 9 and 14 weeks. At each 
date the number of bacteria, amoebae, flagellates, nematodes and mites and the amount 
of mineral nitrogen were measured in three replicates. 
Bacteria were counted by the plate dilution method (medium 1.5% agar, 0.1% glucose, 
0.1% proteose peptone (Prescott and James, 1955). Protozoa were counted by the most-
probable-number method (same medium plus Pseudomonasfluorescens as food) (Darbyshire 
et al., 1974). Nematodes were collected by the elutriation method and then counted 
(Oostenbrink, 1960). Mites were collected by high-gradient extraction and then counted. 
Mineral nitrogen was extracted with IN KCL and determined colorimetrically. 
Role of Soil Fauna in Nutrient Cycling 519 
The numbers of organisms were approximately lognormally distributed, so analyses 
of variance were applied to the log-transformed data. 
RESULTS 
The numbers of the organisms in the four different treatments BP, BPN, BPH and BPNH 
are presented in Fig. 1 and a summary of the analyses of variance is given in Table 1. 
Bacterial numbers were approximately the same in all treatments (Fig la, Table 1). 
Larger numbers of amoebae were found when mites were present (p < 0.001) (Fig. 
1 b). There was an interaction between the effect of nematodes and that of mites on amoebae 
(p < 0.001): the number in the BPNH treatment was lower than in the BPH treatment, 
whereas the number in the BPN treatment exceeded the number in the BP treatment (Fig. 
lb). Comparison of the BPH and the BP treatments, shows that the presence of mites resulted 
in a 15-fold increase in numbers of amoebae. 
Table 1. Effect of nematodes (nema) and mites (mite) on the numbers of bacteria (bact), amoebae (amoe), flagellates 
(flag), nematodes and mites and the amount of mineral N (Nmin) 
Significance 
Nema Mite Nema and mite 
Bact ns ns ns 
Amoe ns <.001 <.001 
Flag <.001 ns <.05 
Nema - <.01 -
Mite ns - -
Nmin <.001 ns <.05 
The number of flagellates was significantly larger in the nematode treatments (p < 0.001, 
Fig. lc). This effect was mainly due to different numbers of flagellates at the beginning 
of the experiment: approximately 500 per g soil in the treatments without nematodes 
compared with 5.15' per g soil in the nematode treatments. The interaction between the 
effect of mites and that of nematodes (p < 0.05) consisted in a slight reduction in the effect 
of nematodes in the presence of mites. 
Mites significantly reduced the number of nematodes (p < 0.01, Fig. Id) by 
approximately 23%. 
Mites were found in smaller numbers when nematodes were present (Fig. le), but this 
difference was not statistically significant. 
Nematodes significantly increased (P < 0.001) the amount of mineral N by approximately 
22%. The effect of mites depended on the presence of nematodes: an increase without 
nematodes (approximately 10%) and no effect when nematodes were present (Fig. If). 
DISCUSSION 
The results show that the system we studied probably consisted of more trophic interactions 
than we assumed before hand (Fig. 2). The stimulating effect of mites on the number of 
amoebae indicates that the feeding rate of the amoebae was increased by mites. The 
accessibility of bacteria to the amoebae may have been improved by H. litorale due to 
the feeding mode of the mite, which cause water currents around its chelicerae (Woodring, 
520 Management and Conservation of Soil Fauna 
(a) bacteria 
Number (IoqiO) per g toil 
(b) amoebae 
Number OoQiO) per g »oil 
0 I 2 3 4 5 « 7 8 9 10 11 12 13 14 0 -o 1 7 3 4 5 e 7 a 9 10 ti n? 13 14 
(c) flagellates 
Number (logiO) per g «oil 
(d) nematodes 
Number U091OI per 100 g »Oil 
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 2 3 4 S 6 7 0 9 10 11 12 13 14 
(e) mites 
Number (k>gi0) per 100 g toil 
(f) mineral N 
Nmtn (mg/kg) 
0 1 2 » 4 S « 7 « f t 1 0 t 1 1 2  1 3  1 4  
Tim« (weeka) 
Fig. 1. Effect of food-web composition on numbers of organisms. 
a. Bacteria, b. Amoebae, c. Flagellates, d. Nematodes, e. Mites, f. Mineral nitrogen. Initial quantities 
are given by the separate points. 
0 : BP: bacteria + amoebae + flagellates 
A : BPN: bacteria, amoebae, flagellates and nematodes 
o : BPH: bacteria, amoebae, flagellates and mites 
V : BPNH: bacteria, amoebae, flagellates, nematodes and mites. 
Each symbol is the mean of three replicates. 
Role of Soil Fauna in Nuirient Cycling 521 
S U B S T R A T E  
B A C T E R I A  
A M O E B A E  J L  F L A G E L L A T E S  N E M A T O D E S  M I T E S  
Kig. 2. Conceptual model of the food web studied: 
Broken line (a) denotes the stimulating effect of mites on consumption by amoebae: broken line <b) 
denotes the feeding on flagellates by amoebae: broken line (c> denotes thai nematodes are accompanied 
by large numbers of flagellates. 
1963). The feeding rate of the flagellates might also have been stimulated by the mites, 
but this fact was possibly obscured by feeding of amoebae on flagellates. 
The presence of large initial numbers of protozoa, especially the flagellates, in the series 
with nematodes indicates that by introducing nematodes we also introduced large numbers 
of protozoa. We also observed that one species of protozoa was present in the treatments 
with nematodes only. 
The reduction of the number of nematodes by mites might be the direct consequence 
of competition between nematodes and mites, but it might also be due to the relatively 
large numbers of amoebae in the mite treatments. Since mites consumed only a small 
proportion of the bacteria in comparison with the amoebae, we attribute the decrease in 
number of nematodes to the large number of amoebae. 
Nematodes increased the number of amoebae in the series without mites, but decreased 
the number of amoebae in the series with mites. These results can be explained by assuming 
a two fold effect of nematodes. Firstly, flagellates may have served as food for the amoebae, 
so that by introducing nematodes accompanied by flagellates, nematodes stimulated the 
growth of amoebae. Secondly, the presence of namatodes and the large numbers of flagellates 
in the nematode treatments decreased the numbers of mites and thereby the positive effect 
of mites on the growth of the amoebae. 
A positive effect of nematodes on nitrogen mineralization is in agreement with 
observations of Anderson et al. (1983) concerning nitrogen mineralization and Coleman 
et al. (1978) concerning soil respiration. In our case the relatively high mineralization rate 
in the nematodes treatment possibly had three causes: (I) the direct effect of the nematodes 
522 Management and Conservation of Soil Fauna 
feeding on bacteria, (II) the large numbers of flagellates accompanying the nematodes 
feeding on bacteria, and (III) the large numbers of flagellates fed upon by the amoebae. 
These flagellates feed on bacteria and are themselves fed upon by amoebae, which thereby 
add to the amount of nitrogen mineralized. 
In summary, the effects of nematodes and mites on the number of amoebae and on 
nitrogen mineralization indicate that mites stimulate the feeding rate of the amoebae and 
that amoebae feed on flagellates. Whether these assumed interactions provide a suitable 
explanation of the experimental findings was examined by means of simulation. Three 
alternative hypotheses were compared. The first included all assumed interaction, i.e. 
amoebae, flagellates, nematodes and mites feeding on bacteria, nematodes "carrying" large 
numbers of flagellates, amoebae feeding also on flagellates and mites stimulating the amoebal 
feeding rate on bacteria. In the second, mites did not stimulate the feeding rate of the amoebae 
and in the third the amoebae did not feed on flagellates. The outcome of this simulation 
showed that only the first hypothesis could account for the observed effects of mites and 
nematodes on the number of amoebae and on the rate of nitrogen mineralization, whereas 
the other two hypotheses, irrespective of the parameter values used, did not generate 
comparable results as were observed in the experiment. 
The results also show that after approximately four weeks all species had reached their 
maximum density, whereas mineralization took place mainly after the fourth week. This 
indicates that nitrogen (and carbon) are not mineralized immediately after feeding. Such 
a time interval between feeding and net mineralization has also been reported for aquatic 
systems with bacterial grazers (Bloem et al., 1988). 
Finally we conclude that a relatively small "pool" of mites may cause a relatively 
large increase of the "flow" of organic material: the amount of organic carbon in the mites 
was approximately 1 |ig per g soil, whereas the mites caused an increase in amoebal carbon 
of approximately 25 ng per g soil. The mites also significantly reduced the stimulating 
effect of the nematodes on the nitrogen mineralization rate. This indicates that in terms 
of both carbon and nitrogen transformations relatively small populations of faunal groups 
may have distinct effects on the functioning of complex ecosystems. 
SUMMARY 
A microcosm experiment was carried out in which we studied the influence of four bacterial 
grazers (amoebae, flagellates, nematodes and mites) on the numbers of bacteria, on the 
numbers of other grazers and on the concomitant nitrogen mineralization. 
Mites increased the number of amoebae. This increase was reduced by nematodes. 
Nematodes increased the number of flagellates and the rate of nitrogen mineralization. Mites 
reduced the positive effect of nematodes on the mineralization rate. 
The results led to the hypothesis that mites promote bacterial consumption by amoebae, 
that nematodes carry protozoa, and that amoebae feed on flagellates. 
ACKNOWLEDGEMENTS 
We thank G.A.J.M. Jagers op Akkerhuis, G. Lebbink, H.G. van Faassen and K.B. Zwart 
for advice, and C.N. Beljaars, E.O. Biewenga and M. ten Cate for technical assistance. 
J.A. van Veen and K.B. Zwart commented on an earlier draft of the manuscript. 
Role of Soil Fauna in Nutrient Cycling 523 
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Population dynamics and nitrogen mineralization rates in soil as influenced by bacterial grazing nematodes and mites

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Population dynamics and nitrogen mineralization rates in soil as influenced by bacterial grazing nematodes and mites

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