Content uploaded by Jean-François Ponge
Author content
All content in this area was uploaded by Jean-François Ponge on Mar 07, 2019
Content may be subject to copyright.
Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil
acidity: interactions with earthworms and predator pressure.
Sandrine SALMON and Jean François PONGE
Laboratoire d’Ecologie Générale, Museum National d’Histoire Naturelle, 4 Avenue
du Petit-Chateau, 91800 Brunoy, France.
Short title: Distribution of Heteromurus nitidus
Number of text pages : 25
5 Tables
2 Figures
Revised on 18th January 99
Softwares used: - Text and tables: Word 97 for Window 95
- Figures: Excel 97 for Window 95
Corresponding author:
Sandrine SALMON
Laboratoire d’Ecologie Générale
Museum National d’Histoire Naturelle
4, Avenue du Petit-Chateau
91800 Brunoy, France
Fax number: +33 1 60465009
E-mail: ssalmon@mnhn.fr
1
Distribution of Heteromurus nitidus (Hexapoda, Collembola) according to soil
acidity: interactions with earthworms and predator pressure.
Sandrine SALMON and Jean François PONGE
Laboratoire d’Ecologie Générale, Museum National d’Histoire Naturelle, 4 Avenue
du Petit-Chateau, 91800 Brunoy, France.
Summary Culture (8 weeks, in sieved fresh humus) and choice (16 weeks in
compartmented boxes containing fresh or defaunated humus, or 5 days on compacted
humus) experiments at varying pH levels demonstrated that the soil-dwelling
Collembolan Heteromurus nitidus (Entomobryomorpha) can live and even prefer
humus with pH<5.0 , contrary to results of field studies. Choice experiments on
moder (pH 7.8) and calcic mull (pH 3.9) showed that H. nitidus was significantly
attracted by the earthworms Allolobophora chlorotica and Aporrectodea giardi
whatever the humus form, except when moder was present on both sides. This
attraction by earthworms may partly explain the field distribution of H. nitidus. A
strong predator pressure was detected in some of the replicates, which seemed to
have an impact on densities and distribution of H. nitidus, as well. Causes of the
attraction by earthworms (food resources, pore size, moisture) are discussed. A
trophic cause is particularly suspected.
2
INTRODUCTION
Soil fauna participate, directly or through their action on microflora, to the
decomposition of litter and to the building of humus profiles (Ponge et al., 1986).
Therefore, the study of the distribution of soil animals is of importance in
characterizing soil-forming processes (Ponge, 1983; Arpin et al., 1984). Among the
large number of factors (e.g. moisture, temperature, light, depth, food resources),
which determine the distribution of soil fauna, humus form (Brêthes et al. 1995) and
soil pH have a marked influence on Collembolan communities (Hågvar and
Abrahamsen, 1984; Ponge, 1993; Klironomos and Kendrick, 1995). Thus, a number
of edaphic Collembolan species may be classified into acid-tolerant and acid-
intolerant species. However, the effect of pH is difficult to identify, because this
measurement is strongly related to humus form, C/N ratio, base saturation and ionic
composition of the soil solution. Some relationships have been found previously
between the abundance of some Collembolan species and base saturation (Ca, Mg,
and Mn ; Hågvar and Abrahamsen, 1984). In fact, the effect of soil pH can be either
direct or indirect. Hågvar (1984) suggested several hypotheses according to which
soil acidity could act through ground vegetation, humus form, predator pressure, food
resources and competition between species. On the other hand, some experimental
studies showed that pH had a strong effect on activity, fecundity, longevity of adults,
and absorption of solutions by the ventral tube (Mertens, 1975; Hutson, 1978;
Jaegger and Eisenbeis, 1984).
According to field studies by Ponge (1983, 1993), Heteromurus nitidus
(Templeton, 1835), an edaphic Collembola (Entomobryidae), was always found in
3
mull humus at pH above 5. This species, which is readily cultured in the laboratory,
was chosen in order to determine whether pH, directly or indirecly, explains
H.nitidus field distribution.
In preliminary experiments we attempted to reproduce in experimental vessels
the results obtained in the field, i.e. to determine whether H. nitidus can live and
reproduce only in a humus at pH>5.0 or if this is a behavioural trait. Results
suggested that earthworms could be implicated in the distribution of H. nitidus. This
hypothesis was further tested by giving H. nitidus a choice between humus
containing or not containing earthworms. The impact of predators was taken into
account in the analysis of results, since it appeared to interact with the above
mentioned factors.
MATERIALS AND METHODS
Preliminary field study
A preliminary study was carried out in the field to see whether H. nitidus was
located only in soils at pH5.0 (Ponge, 1993), when a choice between soils at
different pH levels was offered. The distribution of other Collembolan species
present in the samples was also studied.
Sixty samples were taken in a plot located in the Senart forest near Paris
(France). The soil was a silt-clay loam with a mull humus form under oak (Quercus
petraea), with understory vegetation composed of lime (Tilia cordata), hornbeam
4
(Carpinus betulus) and bramble (Rubus ulmifolius). Varying conditions of soil
acidity have been recorded on this plot, due to the presence of small limestone grains
within a patch approximately 3m diam from which bramble was absent. Twenty
samples of soil+litter were taken with a spade in the central zone without bramble,
and forty samples were taken in the surrounding more acidic zone with bramble. Soil
arthropods were extracted by the dry-funnel method, i.e. animals escape from the
drying sample and are collected at the bottom of a funnel into which they fall.
Determination of Collembola was made at the species level, using a dissecting
microscope (x40) for larger individuals, and under a light microscope (x400) for
smaller ones. Soil pH was measured in a soil/water mixture (1:2 w/w). Data (i.e.
presence of species) were analysed by correspondence analysis (Greenacre, 1984).
This multivariate method permits the simultaneous representation of samples and
species (together with additional variables such as pH) into a plane formed by the
first two factorial axes.
Preliminary culture experiments
The specimens of H.nitidus used in all the experiments arose from cultures on
water-moistened Fontainebleau sand (pure fine quartz sand), fed with a mixture of
terrestrial microalgae (Pleurococcus) and lichens taken from bark scrapings. All
cultures, as well as boxes for choice experiments, were kept at 15°C, under a 10h:14h
light:dark photoperiod.
Two culture experiments, each made of two series of five and three replicates
(one replicate = one box), respectively, were performed using three different types of
5
humus: a calcic eumull (pH 7.2-7.4), an oligomull (pH 4.0-4.6), and an eumoder (pH
4.0-4.3). Classification of humus forms follows Brethes et al. (1995). The eumoder
and the oligomull came from the Senart forest and the calcic eumull came from the
laboratory park (black rendzina under hornbeam). Sampling sites have been
described by Arpin et al. (1984) and Bouché (1975). Fifteen adult or sub-adult H.
nitidus (i.e. specimens 1.8-2.4mm in length according to Krool and Bauer, 1987)
were introduced into circular plastic boxes (8 cm diam, 5 cm height) filled with fresh
roughly sieved (10mm) humus. In one series the individuals were fed with lichens
and microalgae, in the other no food was added. The purpose of this food/no food
comparison was to detect a possible trophic effect on population densities. Cultures
were kept at 15°C for 9 weeks, so that H. nitidus could reproduce several times
(about 3 weeks for an egg-to-egg cycle). Animals were then extracted and counted
and humus pH was measured as described above.
H. nitidus individuals were counted in all replicates. Within each
experimental run, mean numbers of animals in the different substrates were
compared by one-way ANOVA (Sokal and Rohlf, 1995). Data were log-transformed
because the reproduction of animals is a non-linear phenomenon, the variance of
abundances being proportional to their mean. When significant differences among
humus forms were detected, then means were compared by the Newman-Keuls
procedure (Sokal and Rohlf, 1995). The two distinct experimental series were treated
separately because humus sampling was not made at the same time.
Another culture experiment, with three replicates, was performed on
sphagnum moss from the Senart forest. Sphagnum moss is acid (pH 4.0) like
6
eumoder (pH 4.0-4.3) but it is poorer in food resources for Collembola (i.e. absence
of animal faeces and humified organic matter). Fifteen adult H. nitidus were placed
on sphagnum moss, in the same boxes as above and were kept for 9 weeks at 15°C.
The number of individuals was counted at the end of the experiment.
Preliminary choice experiments
Choice experiments were carried out in rectangular boxes (12cm x 18cm x
6.5cm) divided into three compartments by perforated plastic walls. Holes (2mm
diam) allowed free movement by adult H. nitidus. The boxes were placed in a
chamber maintained at 15°C with a 10h:14h day:night photoperiod.
In a first experiment, with three replicates, a fresh sample block of each
humus form, (i.e. oligomull, eumoder or calcic eumull), was placed in each
compartment, the position of the humus changing from a box to another. Eight sub-
adult or adult animals were placed in each compartment, thus 24 individuals were
present in each box. After 9 weeks fauna were extracted separately from each block
of humus. No additional food was supplied. Abundances of H. nitidus in each
compartment were log-transformed and means were compared between humus forms
using two-way ANOVA with experimental boxes as blocks. Humus pH was
measured at the end of the experiment. The same experiment was performed with air-
dried (ambient temperature, 5 months) then remoistened (with deionized water)
humus in order to reduce to a minimum pre-existing fauna without inducing deep
changes in humus characteristics (e.g. pH, organic matter).
7
A third experiment was performed using the same boxes, but filled with
sieved and compacted humus in such a way that H. nitidus could not sink in it. This
allows continuous counting of surface located collembola. Seven sub-adults or adults
were placed in each of the three humus blocks, thus 21 individuals were present in
each box. The abundance of H. nitidus in each compartment was recorded 3 times a
day (at 8h, 13h and 18h) for 5d. Between counting periods boxes were incubated at
15°C. Means of the fifteen countings for each humus form and each box were
compared as described above. A fourth experiment was performed, using fresh
humus blocks (six replicates), as in the first experiment. H. nitidus could only chose
between the two humus forms which differ the most by their pH, i.e. eumoder and
calcic eumull. Thirty adult or sub-adult H. nitidus were evenly distributed on both
humus blocks within each of the six boxes. These were kept for 7d at 15°C, a period
too short for the reproduction of animals, which facilitated counting and avoided log-
transformation of the data. Animals were extracted separately from each block.
Humus pH was measured as above. H. nitidus were counted as were potential
predators of Collembola, i.e. Chilopoda, Pseudoscorpionida, Araneida, and
Formicida (Vannier, 1971; Manley et al., 1976; Bachelier, 1978). The presence of
other fauna (e.g. other collembola species, oribatid mites, Isopoda, Diplopoda) was
noted. Ranked abundances of H. nitidus were compared by Kruskal-Wallis test
(Sokal and Rohlf, 1995). Without reproduction, abundances were too small to allow
variance analysis. Differences in predator numbers between eumoder and calcic
eumull were tested by the same method.
8
Choice experiments with earthworms
The aim of these experiments was to discover if H. nitidus preferred humus
blocks with and without earthworms, independantly of pH or humus form (eumoder
or calcic eumull).
Experimental boxes were divided into two compartments by 1 mm-mesh wire
net to minimize the possibility of earthworms moving from one compartment to the
other. Compartments were filled with blocks of fresh, non sieved humus.
Earthworms were collected in the calcic eumull by expelling them with 4‰ formalin.
The lumbricid community was dominated by Allolobophora chlorotica (Savigny,
1826), a small (50mm), endogeic (soil-dwelling and feeding species) and
Aporrectodea giardi (Savigny, 1826), a large (150 mm) anecic (soil-dwelling species
feeding nightly on litter; Sims and Gerard, 1985). Both species are neutrophilic and
live in soil with little organic matter, but A. giardi is more tolerant to acidity than A.
chlorotica (Bouché, 1972). Because of their large size, we added only one adult A.
giardi to one or both compartments. In one of the experiments, we used two adult A.
chloratica together with one adult A. giardi. All earthworms which had been found
by hand-sorting in humus blocks during field sampling were discarded before the
experimental run. Combinations between humus forms and presence or absence of
earthworms were tested with six replicates each. Thirty adult H. nitidus were added
to each box at the same time earthworms were introduced. Collembola individuals
were distributed in equal number in both compartments. After seven days at 15°C,
animals were extracted in each compartment separately. The abundance of H. nitidus
was estimated as well as that of total predators.
9
Differences between mean abundances of H. nitidus and predators with regard
to presence or absence of earthworms and to humus form were tested by Kruskal-
Wallis test.
RESULTS
Preliminary field study
Table 1 lists the 27 Collembolan species found during the field investigation.
Results of correspondence analysis (Fig. 1) indicate that soil pH, although not
involved as a main variable in the analysis, was strongly correlated with axis 1, with
a highly significant coefficient of determination R2 (P<0.001). Thus the Collembolan
community reflects well the distribution of pH throughout the sampling area, ranging
from 3.9 to 7.4. Axis 1 shows the distribution of several Collembolan species
according to soil pH. Axis 2 has no ecological significance. Sminthurinus signatus
was located in more acidic sites, while H. nitidus, Pseudosinella decipiens, P. alba,
and Folsomides parvulus preferred higher pH soils. Only three H. nitidus individuals
were found in all our samples, all at pH 6 or above. These results corroborated
previous field studies (Ponge, 1993).
Culture experiments
Culture experiments without food supply revealed that H. nitidus reproduces
and survives at pH5.0 and even better than at pH>5, i.e. in oligomull and eumoder
(Table 2). The population in the eumoder (pH 4.0 to 4.2) was three to four times
10
more abundant than in the calcic eumull (pH 7.2 to 7.4) after 9 weeks rearing.
Abundances in the acid mull showed discrepancies between both experiments.
However, the experiments were not run at the same time (the one with three
replicates was in May, the other was in June) and some changes could have occurred
in humus properties, for instance soil pH varied significantly in the oligomull (F test)
between sampling dates. From these first culture experiments we concluded that any
possible pH effect on the field distribution of H. nitidus was indirect. In laboratory
cultures this species not only tolerates acid pH but this condition seems to be more
favourable to its population dynamics than neutral pH, contrary to observations from
field studies.
In cultures with a supply of lichens and microalgae, H. nitidus population
levels largely exceed those obtained in cultures without any food supply, whatever
the pH (Table 2). There were no significant differences between the three humus
forms. However, in the experiment with three replicates, the highest abundance of H.
nitidus was in the calcic eumull. Nevertheless, the residual error was so high and the
degrees of freedom were so small that no difference was significant. The fact that the
influence of humus form disappeared or changed when food was added may
nevertheless suggest that, more important than humus form and acidity, trophic
factors are involved in the distribution of H. nitidus.
In cultures on sphagnum, there were very few H. nitidus (3.7 1.1 individuals
per box) and only adult animals were recovered, indicating that, in addition to the
high mortality rate, no reproduction was occurring. This may be explained by the
11
absence of food available to Collembola, and confirms the involvement of a trophic
factor in the distribution of H. nitidus.
Preliminary choice experiments
Nine weeks choice experiments did not reveal any preference of H. nitidus for
a given humus form, both on fresh and defaunated substrates (Table 3). The
abundance of H. nitidus was much higher (x5.5)on defaunated humus than on fresh
humus, particularly in the oligomull, probably because of the increasing microflora
following remoistening of the air-dried soil (Soulides and Allison, 1961; Scheu and
Parkinson, 1994). Given the long duration of this experiment, considerable
reproduction occurred, and overpopulation may have masked some choice behaviour.
For this reason shorter-term experiments were also performed.
Short-term experiments, where H. nitidus were counted three times a day for
five days on compacted humus, indicated that this species was found more frequently
on eumoder, calcic eumull being the less-preferred humus form (Table 3). These
results confirm the results of culture experiments.
Choice experiments on fresh blocks of eumoder and calcic eumull, where H.
nitidus were counted after seven days, indicated that these animals were significantly
more abundant (P<0.05) in moder (mean pH = 3.9) than in calcic eumull (mean pH =
7.8) which confirmed results from previous three-compartment choices and cultures
(Table 4, "preliminary choice experiment"). In one out of six replicates, H. nitidus
12
was more abundant in calcic eumull. This box was characterized by the presence of
an earthworm.
Choice experiments with earthworms
When H. nitidus could choose between a block with earthworms and a block
without earthworms, their numbers were significantly higher in the block with
earthworms (Table 4). This choice was independent of the humus form
(combinations 1, 2, 3), except in combinations where eumoder was present in both
compartments (combinations 5, 6). Thus H. nitidus was attracted by earthworms or at
least remained longer after random movement in compartments containing
earthworms. When earthworms were present in compartments filled with calcic
eumull and eumoder (combination 4), H. nitidus was not significantly more abundant
in eumoder. Thus the preference for eumoder is real but less strong than the
earthworm effect.
In some replicates we registered a negative relationship between predator and
H. nitidus numbers. In one replicate of combination 3 (Table 4), there were a lot of
ants (92) in the compartment with eumoder and A. giardi, and the abundance of H.
nitidus decreased, contrary to what was found in other replicates (0 or 1 ant).
Moreover, replicates of combination 6 showed a significant (P<0.005) negative
correlation between numbers of H. nitidus and large centipedes (>4 mm) in eumoder
(Fig.2). There was no significant interaction between centipede abundance and the
presence of earthworms (ANOVA). When we compared the number of predators
likely to prey on Collembola, i.e. Chilopoda, Pseudoscorpionida, Araneida and
13
Formicida, in eumoder and calcic eumull (Table 5), we noted that eumoder
accommodated significantly more predators than calcic eumull. The abundance of
predators did not seem to have any effect below a certain threshold which has not
been reached in the calcic mull (Table 5). Therefore the high abundance of predators
of collembola in eumoder (and perhaps in other acid humus forms) could be an
additional reason for the absence of H. nitidus in soils with pH<5.0.
DISCUSSION
In contrast to our field results and those of Ponge (1983, 1993), our culture
and choice experiments showed that H. nitidus prefers acid soils between pH 4 and 5
in which conditions, possibly food resources, are more favourable to its development
than in neutral-alkaline soils. From this it follows that soil acidity (at least at pH 4),
does not have a direct effect on H. nitidus. These results are inconsistent with those
obtained by Kopeszki (1992) in a field experiment, which indicated that the
abundance of H. nitidus decreased according to soil pH-KCl within the range of 4.5
to 3. However, comparison is difficult because experimental conditions as well as pH
measurements were different and, above all, because in Kopeszki's experiments soil
acidification was induced by acid rain, comprising other compounds such as SO42-
which probably had a greater influence than the pH (Sequeira, 1987). Hågvar (1984)
showed that three microarthropod species (including a Collembola species) did not
have the same reaction towards soil pH when they were cultured alone on defaunated
soils compared with cultures in natural soils with complete fauna. Our results support
the hypothesis that other organisms affect the distribution of H. nitidus.
14
The presence of H. nitidus in neutro-alkaline soils only may be determined by
two types of factors: positive factors which attract it to neutro-alkaline and negative
factors which prevent it living in acid soils. In our choice experiments we
demonstrated that H. nitidus moved to compartments with earthworms, the
distribution of which is influenced by soil pH and calcium content (Satchell, 1967;
Piearce, 1972a and 1972b). Piearce (1972b) found earthworms were more important
(in terms of species richness, population density and biomass) in soils > pH5.0
compared to more acidic soils. Moreover, H. nitidus was always found in soils >
pH5.0, thus in mull humus forms. Mull humus forms are rich in earthworms,
particularly earthworms belonging to the anecic ecological category (Jabiol et al.,
1995), while the lumbricid fauna is poorly represented in moder (Bouché, 1975).
Consequently, the distribution of H. nitidus in relation to soil pH is likely to be
controlled by the presence of earthworms. However, this relationship is probably
species-specific since a number of earthworms are acid-tolerant and inhabit oligomull
humus forms at <pH5.0. Aporrectodea giardi and Allolobophora chlorotica, which
attracted H. nitidus in our choice experiments, are considered neutrophilic and live in
soils with little litter (Bouché, 1972). Therefore they will not be present in oligomull.
There is little information about Aporrectodea giardi which occupies a very
restricted geographic area, while Allolobophora chlorotica is an acid-intolerant
species (Piearce, 1972a).
Earthworms have a great impact on the soil environment and therefore the
attraction of H. nitidus to soils containing earthworms may be due to several causes.
Some consider earthworm burrows as a favourable microhabitat for microarthropods,
without distinguishing attractive factors (Bayoumi, 1978; Loksa, 1978). A major
15
initial impact of burrowing is its effect on soil structure (Satchell, 1967). Soil-
dwelling Collembola are sensitive to soil compaction, and any reduction in soil pore
size produces a decrease in Collembola densities (Heisler and Keiser, 1995).
Furthermore, larger Collembola are more abundant in zones with high earthworm
densities than in zones without or with few earthworms (Marinissen and Bok, 1988;
Loranger et al., 1998). Thus earthworm tunnels could allow H. nitidus, a large soil-
dwelling Collembola, to move within the soil profile, either to search for food or to
escape unfavourable conditions near the surface. This would be impossible in moder
where mineral horizons are compact (Bernier, 1996). Some authors assigned the
positive influence of earthworms upon microarthropod populations to improvement
in water retention capacity (Hamilton and Sillman, 1989) or drainage (Loranger et
al., 1998). However, H. nitidus has never been found in oligomull at <pH5, despite
the presence of earthworm burrows.
Our results from culture and choice experiments give more support to a
trophic cause for the attraction of H. nitidus by earthworms, since their gut contents
were mostly made of ingested invertebrate faeces (Arpin et al., 1980; data not
presented). Increase in food availability has been evoked often as an explanation for
the observed impacts of earthworms upon soil fauna (Brown, 1995; Loranger et al.,
1998). Several processes may explain this increase:
(1) Microorganisms. Some bacteria (including actinomycetes) are more abundant in
fresh casts than in surrounding soil (Satchell, 1967; Martin and Marinissen, 1993),
which implies that H. nitidus would have to live in close proximity to earthworms in
order to benefit from fresh cast deposition.
16
(2) Mineral nutrients. Generally, earthworm casts are richer in total and exchangeable
Ca2+, exchangeable K+ and Mg2+, inorganic PO43-, and NO3- (Lunt and Jacobson,
1944; Sharpley and Syers, 1976; Martin and Marinissen, 1993). Acid-intolerant
species of earthworms secrete a greater quantity of calcium than others (Piearce,
1972b; Wiecek and Messenger, 1972).
(3) Organic compounds. Casts and burrow walls have generally a higher content in
organic matter than surrounding soil, at least in deep horizons (Lunt and Jacobson,
1944; Kretzschmar, 1987). Earthworms excrete a number of organic compounds such
as proteins and glycoproteins, urea, amino-acids, vitamins, osides. These are excreted
not only in casts, but also directly in the environment through their nephridiae (El
Duweini and Ghabbour, 1971), and as epidermal mucus which is considered as an
important nitrogen source for soil microorganisms and plants (Needham, 1957;
Dubash and Ganti, 1964; Atlavinyte and Daciulyte, 1969; Cortez and Bouché, 1987).
These products may be different according to species and some of them, particularly
nitrogenous compounds, are susceptible to rapid decomposition, which could
necessit a rapid uptake by H. nitidus, if this species is capable of using them as food.
It is not known whether H. nitidus is attracted to earthworms by chemical
signals or merely remains in a beneficial environment after random exploration of the
soil. The latter process could be reinforced by aggregation pheromones which have
been found in Collembola (Verhoef et al., 1977), including H. nitidus (Krool and
Bauer, 1987). It has been demonstrated that some Collembolan species are attracted
by odours produced by fungal species on which they feed (Bengtson et al., 1988),
which may support the idea of chemoattraction if such odours are produced by
17
earthworms. Furthermore, glycoproteins excreted by Lumbricus terrestris have been
suspected to induce attack by its predators (Halpern et al., 1984).
The attraction of H. nitidus by earthworms may be a reason why this species
is present only in soils at >pH5 but does not explain why it was not found in
oligomull at <pH5 even though it can be cultured in the laboratory in moder at lower
pH. As this research demonstrated, a strong predator pressure has a negative impact
on the presence of H. nitidus. Furthermore, Vannier (1971) noted that ants capture H.
nitidus, and spiders and centipedes are among the most important predators of
Collembola (Manley et al., 1976). In our samples, all three of these predators were
much more abundant in eumoder than in calcic eumull. Thus, predation could explain
the absence of this species at pH<5.
Studying the spatial distribution of soil animals is difficult because several
factors interact with each other (Ponge et al., 1997). In the case of H. nitidus, strong
relationships with earthworms seem established but underlying mechanisms remain
to be studied, as well as quantification of the impact of predators in the field.
18
REFERENCES
Arpin, P., Kilbertus, G., Ponge, J. F. and Vannier, G. (1980) Importance de la
microflore et de la microfaune en milieu forestier. In Actualités d’écologie
forestière, ed. P. Pesson, pp. 87-150. Gauthier-Villars, Paris.
Arpin, P., Ponge, J-F., Dabin, B. and Mori, A. (1984) Utilisation des nématodes
Mononchida et des collemboles pour caractériser des phénomènes
pédobiologiques. Revue d’Ecologie et de Biologie du Sol 21, 243-268.
Atlavinyte, O. and Daciulyte, J. (1969) The effect of the earthworms on the
accumulation of vitamin B12 in soil. Pedobiologia 9, 165-170.
Bachelier, G. (1978) La faune des sols, son écologie et son action. ORSTOM, Paris.
Bayoumi, B. M. (1978) Significance of the microhabitat on the distribution of
oribatid mites in a hornbeam-oak mixed forest. Opuscula Zoologica Budapest
15, 51-59.
Bengtsson, G., Erlandsson, A. and Rundgren, S. (1988) Fungal odour attracts soil
Collembola. Soil Biology and Biochemistry 20, 25-30.
Bernier, N. (1996) Altitudinal changes in humus form dynamics in a spruce forest at
the montane level. Plant and Soil 178, 1-28.
Bouché, M. B. (1972) Lombriciens de France. Ecologie et systématique. I.N.R.A.
Publ. 72-2, Paris.
Bouché, M. B. (1975) Fonctions des lombriciens. III. Premières estimations
quantitatives des stations françaises du P.B.I. Revue d’Ecologie et de Biologie
du Sol 12, 25-44.
19
Brêthes, A., Brun, J. J., Jabiol, B., Ponge, J. F., and Toutain, F. (1995) Classification
of forest humus forms: a French proposal. Annales des Sciences Forestières
52, 535-546.
Brown, G.G. (1995) How do earthworms affect microfloral and faunal community
diversity? Plant and Soil 170, 209-231.
Cortez, J. and Bouché, M. (1987) Composition chimique du mucus cutané de
Allolobophora chaetophora chaetophora (Oligochaeta: Lumbricidae).
Comptes-Rendus de l’Académie des Sciences de Paris, Série III, 305, 207-
210.
Dubash, P. J. and Ganti, S. S. (1964) Earthworms and amino-acids in soil. Current
Science 7, 219-220.
El Duweini, A. K. and Ghabbour, I. (1971) Nitrogen contribution by live earthworms
to the soil. IVth Colloquium Pedobiologiae, 1970, September, Dijon, France,
pp 495-501. INRA, Paris.
Greenacre, M. J. (1984) Theory and applications of correspondence analysis.
Academic Press, London.
Hågvar, S. (1984) Ecological studies of microarthropods in forest soils, with
emphasis on relations to soil acidity. University of Oslo, Oslo.
Hågvar, S. and Abrahamsen, G. (1984) Collembola in Norwegian coniferous forest
soils. III. Relations to soil chemistry. Pedobiologia 27, 331-339.
Halpern, N., Schulman, N., Scribani, L. and Kirschenbaum, D. M. (1984)
Characterization of vomeronasally-mediated response-eliciting components of
earthworm wash. II. Pharmacology, Biochemistry and Behavior 21, 655-662.
Hamilton, W. E. and Sillman, D. Y. (1989) Influence of earthworm middens on the
distribution of soil microarthropods. Biology and Fertility of Soils 8, 279-284.
20
Heisler, C. and Keiser, E. A. (1995) Influence of agricultural traffic and crop
management on collembola and microbial biomass in arable soil. Biology and
Fertility of Soils 19, 159-165.
Hutson, B. R. (1978) Influence of pH, temperature and salinity on the fecundity and
longevity of four species of Collembola. Pedobiologia 18, 163-179.
Jabiol, B., Brêthes, A., Ponge, J. F., Toutain, F. and Brun, J. J. (1995) L'humus sous
toutes ses formes. ENGREF, Nancy.
Jaeger, G. and Eisenbeis, G. (1984) pH-dependent absorption of solutions by the
ventral tube of Tomocerus flavescens (Tullberg, 1871) (Insecta, Collembola).
Revue d’Ecologie et de Biologie du Sol 21, 519-531.
Klironomos, J. N. and Kendrick, B. (1995) Relationships among microarthropods,
fungi and their environment. Plant and Soil 170, 183-197.
Kopeszki, H. (1992) Versuch einer aktiven Bioindikation mit den bodenlebenden
Collembolen-Arten Folsomia candida (Willem) und Heteromurus nitidus
(Templeton) in einem Buchenwald-Ökosystem. Zoologischer Anzeiger 228,
82-90.
Kretzschmar, A. (1987) Caractérisation microscopique de l'activité des lombriciens
endogés. In Micromorphologie des sols. Soil micromorphology, eds. N.
Fedoroff, L. M. Bresson, and M. A. Courty, pp. 325-330. AFES, Paris.
Krool, S. and Bauer, T. (1987) Reproduction, development and pheromone secretion
in Heteromurus nitidus Templeton, 1835 (Collembola, Entomobryidae).Revue
d’Ecologie et de Biologie du Sol 24, 187-195.
Loksa, I. (1978) Mikrohabitate und ihre Bedeutung für die Verteilung der
Collembolengemeinschaften in einem Hainbuchen- Eichenbestand. Opuscula
Zoologica Budapest 15, 93-117.
21
Loranger, G., Ponge, J. F., Blanchart, E. and Lavelle, P. (1998) Impact of earthworms
on the diversity of microarthropods in a vertisol (Martinique). Biology and
Fertility of Soils 27, 21-26.
Lunt, H. A. and Jacobson, H. G. M. (1944) The chemical composition of earthworm
casts. Soil Science 58, 367-375.
Manley, G. V., Butcher, J. W. and Zabik, M. (1976) DDT transfer and metabolism in
a forest litter macro-arthropod food chain. Pedobiologia 16, 81-98.
Marinissen, J. C. Y. and Bok, J. (1988) Earthworm-amended soil structure: its
influence on Collembola populations in grassland. Pedobiologia 32, 243-252.
Martin, A. and Marinissen, J. C. Y. (1993) Biological and physico-chemical
processes in excrements of soil animals. Geoderma 56, 331-347.
Mertens, J. (1975) L’influence du facteur pH sur le comportement de Orchesella
villosa (Geoffroy , 1764), (Collembola, Insecta). Annales de la Société Royale
de Zoologie de Belgique 105, 45-52.
Needham, A. E. (1957) Components of nitrogenous excreta in the earthworms
Lumbricus terrestris L. and Eisenia foetida (Savigny). The Journal of
Experimental Biology 34, 425-446.
Piearce, T. G. (1972a) Acid intolerant and ubiquitous Lumbricidae in selected
habitats in North Wales. The Journal of Animal Ecology 41, 397-410.
Piearce, T. G. (1972b) The calcium relations of selected Lumbricidae. The Journal of
Animal Ecology 41, 167-188.
Ponge, J. F. (1983) Les collemboles indicateurs du type d’humus en milieu forestier.
Résultats obtenus au Sud de Paris. Acta Oecologica 4, 359-374.
Ponge, J. F. (1993) Biocenoses of Collembola in atlantic temperate grass-woodland
ecosystems. Pedobiologia 37, 223-244.
22
Ponge, J. F., Arpin, P., Sondag, F. and Delecour, F. (1997) Soil fauna and site
assessment in beech stands of the Belgian Ardennes. Canadian Journal of
Forest Research 27, 2053-2064.
Ponge, J. F., Vannier, G., Arpin, P. and David, J. F. (1986) Caractérisation des
humus et des litières par la faune du sol. Intérêt sylvicole. Revue Forestière
Française 38, 509-516.
Satchell, J. E. (1967) Lumbricidae. In Soil biology, eds. A. Burges and F. Raw,
pp259-322. Academic Press, London.
Scheu, S. and Parkinson, D. (1994) Changes in bacterial and fungal biomass C,
bacterial and fungal biovolume and ergosterol content after drying,
remoistening and incubation of different layers of cool temperate forest soils.
Soil Biology and Biochemistry 26, 1515-1525.
Sequeira, R. (1987) The chemical nature of acid precipitation over Europe. Current
Science 56, 514-517.
Sharpley, A. N. and Syers, J. K. (1976) Potential role of earthworms casts for the
phosphorus enrichment of run-off waters. Soil Biology and Biochemistry 8,
341-346.
Sims, R. W. and Gerard, B. M. (1985) Earthworms. Keys and notes for the
identification and study of the species. Linnean Society of London, London..
Sokal, R. R. and Rohlf, F. J., (1995) Biometry. 3rd edition. W.H. Freeman and
Company, New York.
Soulides, D. A. and Allison, F. E. (1961) Effect of drying and freezing soils on
carbon dioxide production, available mineral nutrients, aggregation, and
bacterial population. Soil Science 91, 291-298.
23
Vannier, G. (1971) Les fourmis, prédateurs permanents de certains types de
collemboles. Revue d’Ecologie et Biologie du Sol 8,119-132
Verhoef, H. A., Nagelkerke, C. J. and Joosse, E. N. G. (1977) Aggregation
pheromones in Collembola (Apterygota), a biotic cause of aggregation. Revue
d’Ecologie et de Biologie du Sol 14, 21-25.
Wiecek, C. S. and Messenger, A. S. (1972) Calcite contributions by earthworms to
forest soils in northern Illinois. Soil Science Society of America Proceedings
36, 478-480.
24
LEGENDS
Fig. 1 Correspondence analysis on 60 field samples from the Senart forest and 27
Collembolan species. Projection in the plane of axes 1 and 2. Collembolan species
are coded by three letters. = soil with limestone grains, = surrounding acid soil.
Fig. 2 Linear regression between densities of H. nitidus and big-size centipedes (>4
mm) in combination 6 of choice experiments with earthworms (see text).
25
Table 1. List of Collembolan species found in the field study and represented in the correspondence
analysis (Fig. 1)
AFU
Allacma fusca (Linné, 1758)
ATE
Arrhopalites terricola (Gisin, 1958)
DMI
Dicyrtomina minuta (Fabricius, 1783)
EMU
Entomobrya multifasciata (Tüllberg,1871)
FMA
Folsomia manolachei (Bagnall, 1939)
FPA
Folsomides parvulus (Stach, 1922)
HMA
Heteromurus major (Moniez, 1889)
HNI
Heteromurus nitidus (Templeton, 1835)
IMI
Isotomiella minor (Schäffer, 1896)
LCU
Lepidocyrtus curvicollis (Bourlet, 1839)
LLA
Lepidocyrtus lanuginosus (Gmelin, 1788)
MMI
Megalothorax minimus (Willem, 1900)
MMA
Mesaphorura macrochaeta (Rusek, 1976)
NMU
Neanura muscorum (Templeton, 1835)
OIN
Onychiurus insubrarius (Gisin, 1952)
OCI
Orchesella cincta (Linné, 1758)
OVI
Orchesella villosa (Geoffroy, 1764)
PCA
Paratullbergia callipygos (Börner, 1902)
PNO
Parisotoma notabilis (Schäffer, 1896)
PAL
Pseudosinella alba (Packard, 1873)
PDE
Pseudosinella decipiens (Denis, 1924)
SSI
Sminthurinus signatus (Krausbauer, 1898)
SIN
Undetermined Symphypleona
TBO
Tomocerus botanicus (Cassagnau, 1962)
VAR
Vertagopus arboreus (Linné, 1758)
XGR
Xenylla grisea (Axelson, 1900)
XAR
Xenyllodes armatus (Axelson, 1903)
26
Table 2. Densities of H.nitidus in culture experiments on three humus forms at different pH values.
CM: calcic eumull, AM: oligomull, MO: eumoder. SEM: standard error of the mean. ANOVA was
performed on log-transformed data. A posteriori comparisons (Newman-Keuls test) were done at 0.05
level
Cultures
Number
of
Replicates
Densities of H. nitidus
in each humus form
(mean ± SEM)
F value
(ANOVA
)
Probability
Newman-Keuls
test
Without
3
CM (pH 7.39) : 7.3 ± 3.2
AM (pH 4.64) : 25.3 ± 2.9
MO (pH 4.00) : 21.7 ± 1.9
6.41
0.0328
MO=AM>CM
food supply
5
CM (pH 7.24) : 12.6 ± 5.7
AM (pH 4.11) : 9.8 ± 2.6
MO (pH 4.23) : 28.0 ± 3.7
4.81
0.0290
MO>CM=AM
With
3
CM (pH 7.40): 2374.3 ± 249.7
AM (pH 4.43) : 348.3 ± 116.0
MO (pH 4.04) : 504.3 ± 250.9
3.29
0.1079
food supply
5
CM (pH 7.27) : 2658.0 ± 621.9
AM (pH 4.05) : 1883.6 ± 249.7
MO (pH 4.27) : 2485.6 ± 255.4
0.48
0.6326
27
Table 3. Densities of H.nitidus (mean of three replicates) in preliminary choice experiments using
three humus forms at different pH values. CM: calcic eumull, AM: oligomull; MO: eumoder. SEM:
standard error of the mean. A posteriori comparisons (Newman-Keuls test) were done at 0.05 level
Choice
Experiments
H. nitidus number
in each humus type
(mean ± SEM)
F value
(ANOVA)
Probability
Newman-Keuls
test
25 H. nitidus
on fresh
humus
CM (pH 7.51) : 54.7 ± 7.9
AM (pH 4.32) : 64.0 ± 22.2
MO (pH 3.87) : 40.7 ± 6.2
0.16
(log-transformed
data)
0.8562
for 2 months
on dried and
remoistened
humus
CM (pH 7.42) : 185.3 ± 42.0
AM (pH 4.75) : 458.3 ± 99.7
MO (pH4.32) : 250.7 ± 10.1
5.29
(log-transformed
data)
0.0763
20 H. nitidus for 5 days
on compacted humus
CM : 4.58 ± 0.5
AM : 5.96 ± 0.4
MO : 8.64 ± 0.4
(Mean of
15 countings)
26.35
0.000
MO>AM>CM
28
Table 4. Distribution of H. nitidus with regard to the presence of earthworms and to humus form.
Each combination was run with 6 replicates and 30 adults. CM: calcic eumull, MO: eumoder, NS: not
significant
Combination
Blocks
Densities of H.
nitidus (mean of
replicates/block)
X² test
(Kruskal-Wallis)
Preferred block
Preliminary
choice
experiment
MO without earthworms
17
P<0.05 (P<0.01 without the
replicate containing an
earthworm in CM)
MO
CM without earthworms
except in one replicate
7
1
CM + A. giardi
25
P<0.005
CM + A. giardi
CM without earthworms
3
2
CM + A. giardi
28
P<0.005
CM + A. giardi
MO without earthworms
3
3
CM without earthworms
7
P<0.05 (P<0.001 without the
replicate containing 92 ants)
MO + A. giardi
MO + A. giardi
19
4
MO + A. giardi
15
NS
CM + A. giardi
9
5
MO + A. giardi
14
NS
MO without earthworms
9
6
MO + A. giardi + A.
chloratica
17
NS
MO without earthworms
12
29
Table 5. Densities of predators (Chilopoda, Pseudoscorpionida, Araneida and Formicida) in choice
experiments with regard to humus form and presence of earthworms. Each combination was run with
6 replicates. CM: calcic eumull, MO: eumoder.
Combination
Blocks
Densities of predators
(mean of
replicates/block)
X² test
(Kruskal-Wallis)
Humus with the
highest predator
number
Preliminary
choice
experiment
CM without earthworms
except in one replicate
1.33
P<0.005
MO
MO without earthworms
7.50
2
CM + A. giardi
1.33
P<0.05
MO
MO without earthworms
5.50
3
CM without earthworms
0.83
P<0.005
MO
MO + A. giardi
20.50
4
CM + A. giardi
1.00
P<0.005
MO
MO + A. giardi
9.00
30
AFU
ATE
DMI
EMU
FMA
FPA
HMA
HNI
IMI
LCU
LLA
MMI
MMA
NMU
OIN
OCI
OVI
PCA
PNO
PAL
PDE
SSI
SIN
TBO
VAR
XGR
XAR
pH+
pH-
2
1
Fig. 1
31
R² = 0.678
0
5
10
15
20
25
30
0 2 4 6 8 10 12 14 16
Abundance of H.nitidus
Abundance of Centipedes
Fig. 2
