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Geoderma, 49 ( 1991 ) 33-62 33
Elsevier Science Publishers B.V., Amsterdam
Food resources and diets of soil animals in a small
area of Scots pine litter
J.F.
Ponge
Museum National d'Histoire Naturelle, Laboratoire d'Ecologie G#n~rale, 4 Avenue du Petit-Chateau,
F-91800 Brunoy, France
(Received April 26, 1990; accepted after revision October 17, 1990 )
ABSTRACT
Ponge, J.F., 199 I. Food resources and diets of soil animals in a small area of Scots pine litter. Geo-
derma, 49" 33-62.
The fauna inhabiting a small area (ca. 5 cmX 5 cm) were investigated in a Scots pine stand. After
microstratification of the litter layers in the field and fixation in 95% ethyl alcohol, invertebrates,
mainly mesofauna, were sorted under a dissecting microscope and mounted or dissected in order to
study their intestinal guts. Faeces were mounted or sectioned to obtain information about the activity
of other invertebrate groups not represented in the sample and to follow the fate of plant and micro-
bial material after defaecation occurred.
Plant material, mainly from moss, bracken, pine needles and bark, was extensively consumed by
enchytraeid and lumbricid worms, sciarid larvae and phthiracarid mites. Fungal material was in-
gested by all groups, either in combination with plant material or alone (camisiid and oppiid mites,
some species of Collembola, sciarid and chironomid larvae). Isotomid springtails and chironomid
larvae appeared to consume faecal material. The choice and the degree of comminution and digestion
of the material differed greatly from one group to another, but without any indication of resource
sharing.
INTRODUCTION
The role of fauna in forest soils has been the subject of many investigations.
Despite their low contribution to total soil metabolism (Macfadyen, 1963 ),
invertebrates are known to influence microbial populations, and hence indi-
rectly affect total metabolism, by regulating fungal growth (Warnock et al.,
1982; Ulber, 1983; Gochenaur, 1987), disseminating fungal and bacterial
propagules into new substrates (Visser et al., 1981 ) or reactivating senescent
microbial colonies (Hanlon, 1981 ). The net effect of these activities appears
to depend on the density of animals and conditions for the development of
microflora (Wolters, 1988 ). The importance of soil fauna in the development
of soil structure can be seen as channels and faecal deposits throughout the
0016-7061/91/$03.50 © 1991 -- Elsevier Science Publishers B.V.
34 J.F. PONGE
humus profile (Kubifina, 1943, 1955; Zachariae, 1965; Bal, 1970; Babel, 1975;
Bal, 1982; Kretzschmar, 1987).
Microscopic investigations in a small volume of soil (Ponge, 1984, 1985a,b,
1988, 1990, in prep. ) helped us to understand some functional relationships
between soil animals, soil microflora and the living and dead plant material
in the top centimeters of a moder humus. Results for fauna are presented
here, and the ecology and ecological effects of soil and litter invertebrates are
discussed.
MATERIAL AND METHODS
A unique sample was taken in August 1981 from a 35 yr old Scots pine
(Pinus sylvestris
L. ) stand in the Orleans Forest (Loiret, France), which had
not been thinned until the time of sampling. The ground flora mainly con-
sisted of the moss
Pseudoscleropodium purum
(L.) and bracken
(Pteridium
aquilinum
(L.). The humus was of the moder type ( Ponge, 1984 ). Microstra-
tification of the surface horizons was made in the field on an area of ca. 5
cm X 5 cm. Only the first three sub-layers were intensively studied, LI (entire
brown needles, living mosses ), L2 (entire black needles, dead mosses ) and FI
(fragmented needles, roots, fungi and animal faeces). These layers corre-
sponded to the Ln, Lv and
Fr
sub-layers (sensu Babel, 1971 ). After dissecting
the plant material out of the woodland floor it was immediately fixed in 95%
ethyl alcohol. In the laboratory, plant fragments, animals and faeces were
sorted under a dissecting microscope and appropriate techniques were used
for their study (Ponge, 1984). Most animals were mounted intact under a
cover slide into chlorallactophenol (25 cm 3 lactic acid+50 g chloral hy-
drate+ 25 cm 3 phenol). Oribatid mites, which had a thicker tegument, were
dissected and the cuticles discarded, but the small
Oppia
species were mounted
whole. The volume of each individual was estimated by means of three mea-
surements [length, width and thickness, see Ponge (1984) for further details ].
All animal groups (mainly mesofauna and macrofauna ) present at the time
of sampling were collected. Microfauna (protozoans, nematodes, rotifers)
were poorly recovered, as a consequence of their small size and transparency.
Animals that were living inside plant material (phthiracarid larvae, nema-
todes, amoebae) were also underinvestigated.
Unless otherwise stated, phase contrast microscopy was used to study gut
contents. The presence of intact cytoplasm in the ingested cells was detected
through its opacity (Frankland, 1974).
VERTICAL DISTRIBUTION OF INVERTEBRATES
Figure 1 indicates the density and body volume of the five main meso-
faunal groups recorded in the three litter layers. The sampled surface was ap-
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 35
~400] L1 L2
I ENCHYTREIDS
ORI BATID MITES ~ L L
MISCELLANEOUS .~
MITES
SPRI NGTAILS
FLY LARVAE 0
"~ 20
I
Fig. 1. Population density and bio-volume (upper estimate, see text) of the five main meso-
faunal groups in the L~, L2 and F~ layers.
proximately 0.25 dm 2. The volume estimate which was used for the animals
was V~ (Ponge, 1984), i.e., the upper estimate (animals were compared to a
parallelepipedic volume having the same dimensions). The true volume falls
within a range from 0.25 V~ to V~.
A marked increase in total density and bio-volume of fauna from the L to
the F layers was observed. This was mainly due to enchytraeid worms, mites
and springtails (Collembola). Unlike enchytreids whose numbers regularly
increased from LI to FI, oribatid mites decreased from L1 to L2 then increased
to FI. Collembola were numerous only in the F~ layer. Within each group, the
species composition of the layers differed except for enchytraeids represented
by the single species
Cognettia sphagnetorum
(Vejd.). Oribatids were domi-
nated by camisiid species in the L layers and by phthiracarid species in the F,
layer (Ponge, 1984, 1985a, 1988). Springtails were dominated by isotomid
species in all layers. Diptera larvae were dominated by a cecidomyid species
in the L, layer, and by a sciarid species in the two other layers.
The groups which played a prominent role in the decomposition process of
plant material were enchytraeids, phthiracarid mites, sciarid larvae and epi-
geous earthworms (Ponge, in prep. ). The three former groups actively tun-
nelled through pine needles and pieces of bark (Figs. 2 and 3 ), and the earth-
worms crushed the needles after ingestion of entire fragments.
36 J.F. PONGE
2ram
Fig. 2. Oribatid faecal pellets at the inside of a pine needle (after partial dissection ). Ft layer.
Fig. 3. Two enchytraeid worms (Cognettia sphagnetorum) tunnelling through the same pine
needle, indicated by arrows (pellets have been deposited at the outside). F~ layer.
FOOD RESOURCES AND THEIR FATE IN ANIMAL GUTS AND FAECES
Table 1 summarizes ingestion of the different food resources by the ob-
served animal groups, and their fate in the guts or faeces. Digestion or trans-
formation refers to cell walls, since cytoplasm was always digested. Observa-
tions of intact plant and fungal material were made to facilitate the
identification of material in guts and faeces. The treatise on plant anatomy
by Esau (1965) was used as a reference for nomenclature of higher plant
tissues.
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
TABLE 1
Food resources and their ingestion by animal groups.
37
Food Enchy- Sciarids Oribatids
traeids Phthir. Others
Springtails Earthworms Woodlice Slugs
Pine needles * *(D) *(T)
Pine resin *
Pine pollen *(D) *
Pine wood *
Pine bark *
Bracken *
Moss living * *
Moss dead *
Fungus hyaline * ( D ) *
Fungus dematiaceous *
Cyanobacteria *
Algae * ( D )
Bacteria
Faeces * *
Testacea * (D)
*(D)
*(T)
* = Ingested; D = digested; T = transformed.
Fig. 4. Protoxylem reticulate tracheid (arrow 1 ) and dissociated cell walls (arrow 2) from pine
needles in the gut of an enchytraeid worm. Same species as above. L2 layer. Phase contrast.
Bar= 50 I~m.
Plant tissues from pine needles were identified in the guts through the pres-
ence of lignified tissues such as tracheids from protoxylem (Fig. 4) and me-
taxylem. The transfusion tissue of pine was characterized by an accumulation
of bordered pits (Fig. 5 ). Other hard structures, such as guard cells of stomata
38 J.F. PONGE
Fig. 5. Accumulation of bordered pits (arrow 1 ) from pine transfusion tissue (stele parenchym
of needles) and emptied basidiomycete hyphae (arrow 2) in the gut of an enchytraeid worm.
Same species as above F~ layer. Phase contrast. Bar= 50 ~tm.
Fig. 6. Faecal pellet, attributed to a woodlouse. Pine needles, cutted into small pieces and com-
pacted. F~ layer.
and epidermis, were used to identify material derived from pine needles. Pine
needles were ingested by all groups except springtails and oribatid mites other
than phthiracarids. Digestion occurred only in the intestine of sciarid larvae.
In the post-colon of phthiracarid mites the plant cell walls were observed be-
coming brownish and their structure amorphous, especially at the center of
the food pellets. The feeding activities of other animal groups was followed
through their faecal pellets (Figs. 6-8 ).
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 39
Fig. 7. Faecal material, attributed to a slug. Pine needles, ingested as entire or large pieces. F~
layer.
Fig. 8. Pine needle mesophyll in the abovementioned faecal material. Cells have their wall in-
tact, but their content has disappeared. F~ layer. Phase contrast. Bar = 50 ~tm.
The moss
Pseudoscleropodium purum
was consumed by animals both in the
living state (L1 layer) and after invasion by fungi (F1 layer). Thus, in the L2
layer, where moss was dead but relatively free. of fungal hyphae, it was very
rarely encountered in animal guts and faeces.
Pine resin was ingested by enchytraeids (Fig. 9), which were often found
between bark and wood in fallen twigs and branches. This material was never
observed in any other group and the degree to which the worms deliberately
ingested resin, and were able to digest it, is unknown.
40 J.F. PONGE
Fig. 9. Resin pieces in the gut of the enchytreid worm Cognettia sphagnetorum. L 2 layer. Phase
contrast. Bar= 50 rtm.
Fig. 10. Two pine pollen grains (exin) in the gut of the same species. L~ layer. Phase contrast.
Bar-- 50 ~tm.
Pollen grains from pine were commonly encountered in the food bolus of
many enchytraeids (Figs. 10 and 1 1 ) and Sciarids (Fig. 12) and in earth-
worm faeces. Lysis of the more resistant surface layers of pollen grains was
observed in the gut of enchytraeid worms. In every case, pollen grains were
ingested mixed with many other materials, since this food resource was finely
dispersed throughout the litter.
Soil fungi were the resource the most widely selected by soil animals. Fun-
gal material, predominantly hyphae, were observed in the guts of all observed
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 41
Fig. 11. Fragment of a pine pollen grain (exin, arrow 1 ), together with fungal wall remnants
(arrow 2) and bacteria in the gut of the same species. L2 layer. Phase contrast. Bar= 50 p.m.
Fig. 12. Pine pollen grain (exin) in the gut ofa sciarid larva. L1 layer. Phase contrast. Bar=
50
p.m.
animals except starved (moulting) individuals. Hyaline hyphae were the most
abundant form in this soil volume. Most of them were produced by a mycor-
rhizal basidiomycete, belonging probably to the genus
Hyphodontia
(Ponge,
1988 ). It also colonized dead pine wood in our sample. Hyphae of this fungus
were observed to be connected to the pine root system (orange-brown coral-
loid mycorrhizae) and to penetrate the litter (Ponge, 1990). These hyphae
were found in the guts of enchytraeid worms, where they appeared to be more
or less digested (Fig. 13 ). Hyphae covered with oxalate crystals were egested
42 J.F. PONGE
Fig. 13. Hyaline hyphae partially digested in the gut of the enchytraeid worm
Cognettia sphag-
netorum.
Compare with intact cell walls of the mycorrhizal fungus
Cenococcum geophilurn (ar-
row). L2 layer. Phase contrast. Bar= 50 lain.
Fig. 14. Hyphae of two mycorrhizal fungi,
Cenococcum geophilum (melanized
walls, arrow 1 )
and
Hyphodontia
sp. (hyaline hyphae, arrow 2) in the gut of the springtail
Pseudosinella terri-
cola.
Only the hyaline hyphae were being digested. F~ layer. Phase contrast. Bar = 50 ~tm.
as compacted masses once the chitinous wails had been fully digested. In ori-
batid mites, hyaline hyphae of
Hyphodontia
were observed in the genus
Op-
pia,
where digestion commonly occurred, and in several other species where
digestion did, or did not, occur (Ponge, 1988). Some species of Collembola
fed on this fungus, such as
Pseudosinella terricola
Gisin, 1967 (Fig. 14 ),
Wil-
lemia anophthalma
B6rner, 1901 and
Pogonognathellusflavescens
(Tullberg,
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
43
1871 ). In every case digestion occurred, except for the oxalate crystals. Sciarid
larvae did not appear to be able to digest hyaline fungal walls, since these
hyphae were always present without any change in their appearance (Fig. 15 ),
but the opacity of the cytoplasm had disappeared (when observed in phase
contrast microscopy), indicating that only the cell contents were used by these
animals. Hyaline hyphae were also ingested by members of the macrofauna,
together with plant material, but unfortunately the feeding behaviour of these
animals was observed only through their faeces. Since it was virtually impos-
sible to discriminate between fungi colonizing faecal masses and those in-
gested with the original food material we could not reach a conclusion on this
point.
Dematiaceous (melanine stained) fungi were present mainly in the form
of the dark mycelium of the sterile mycorrhizal ascomycete
Cenococcum geo-
philum
Fr. A broad spectrum of animal species was also feeding on this fun-
gus (as specialized feeders or not), but, contrary to the aforementioned hya-
line basidiomycete, the digestion of the hyphal walls of this fungus seemed
difficult or even quite impossible for most groups. Dematiaceous hyphal walls
remained intact in enchytraeid worms (Figs. 16, 13: compare to hyaline hy-
phae ). In some cases, some signs of attack were visible, such as small holes in
the thick walls of this fungus (Fig. 17 ), but this was probably due to the action
of bacteria or amoebae prior to ingestion by the animal. More pronounced
features were also observed, which might be due to the action of gut enzymes.
In some other cases, where decay was still more pronounced, we hypothesize
that the dematiaceous material had been already ingested by another animal
and was present as faeces in the food bolus of enchytraeids. Dematiaceous
Fig. 15. Hyaline hyphae of the mycorrhizal fungus
Hyphodontia
sp., with intact cell walls (ar-
row), in the gut ofa sciarid larva. L2 layer. Phase contrast. Bar= 50 ~tm.
44
J.F. PONGE
Fig. 16. Melanized hyphae of the mycorrhizal fungus
Cenococcum geophilum,
with intact cell
walls, in the gut of the enchytraeid worm
Cognettia sphagnetorum.
L~ layer. Phase contrast.
Bar= 50 lam.
Fig. 17. Same material in the same animal species as above. Note small holes (arrows) in else-
where intact cell walls.
L 2
layer. Phase contrast. Bar= 50 Ixm.
hyphae and spores were present in the food bolus of oribatid mites, mainly
camisiid species such as
Platynothrus peltifer
(Koch, 1839 ) and
Nothrus syl-
vestris (Koch,
1839) and were also observed in faecal pellets (Fig. 18 ). Ob-
servation of faeces indicated that some transformation in plant tissue struc-
ture occurred, especially at the centre of the pellets, but this was not observed
inside animal guts.
Filamentous cyanobacteria were found in enchytreid guts. Digestion was
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
45
Fig. 18. Melanized hyphae, with intact cell walls, of the mycorrhizal fungus
Cenococcum
geo-
philum,
in an oribatid faecal pellet. L2 layer. Phase contrast. Bar= 50 p,m.
Fig. 19. Filamentous cyanobacteria during their digestion in the gut of the enchytraeid worm
Cognettia sphagnetorum.
Cells (arrows) have been separated and emptied. In other respects
same as Fig. 18.
followed by comparing several parts of the same animal intestine: cells were
separated then emptied (Fig. 19), with the cellulosic walls remaining
untouched.
Unicellular algae were often found in the guts of enchytraeids (Fig. 20).
Viability of the cells was recognized by opacity of their cytoplasm when ob-
served in phase contrast. The presence of intact cells inside the intestine in-
dicated that digestion of algae seemed to be somewhat difficult. Nevertheless
46 J.v. PONGE
Fig. 20. Chlorella-like algae in the gut of the same species. Intact cells, with opaque cytoplasm.
In other respects same as Fig. 18.
! ii!!!~!i~ :i(i~ ¸¸
Fig. 21. Digestion of Chlorella-like algae in the gut of the same species. Covering of the cells
with symbiotic bacteria ( 1 ) was followed by loss of cytoplasm opacity (2) then by collapsing
( 3 ). L2 layer. Phase contrast. Bar= 50/am.
digestion occurred with the help of intestinal microflora (Fig. 21 ): cells were
( 1 ) coated with bacteria, then (2) their cytoplasm disappeared, and (3) they
collapsed. One species of Collembola, Lepidocyrtus lanuginosus (Gmelin,
1788 ) seemed to digest algae more easily, since no opacity was found in the
cells (Fig. 22 ). Some cell walls were seen to be partially digested but, unfor-
tunately, the few animals collected of this species made it impossible to con-
clude that digestion of the walls was always occurring. In this collembolan,
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
47
Fig. 22. Soil algae, without cell contents, in the gut of the springtail
Lepidocyrtus lanuginosus.
F~ layer. Phase contrast. Bar= 50 pm.
death of the algae was only due to the action of the animal: no associated
bacteria were found in the intestine of Collembola, contrary to other animal
groups as will be seen below (and confirmed in transmission electron micros-
copy by Saur and Ponge, 1988 ).
Bacteria were present in a lot of plant fragments that were ingested both by
macrofauna and mesofauna (especially pine needles in the L2 layer, Ponge,
1985a), but in this case their fate was not easy to discern. Nevertheless it
must be noticed that the food bolus of the collembolan species
Megalothorax
minimus
(Willem, 1900) was always made of bacteria mixed with minute
fungal and mineral particles (Fig. 23 ).
Faecal material was seemingly the main food of some species of Collembola
belonging to the same family (Isotomidae), namely
Folsomia manolachei
Bagnall, 1839 (=F.
nana), Parisotoma notabilis
(Sch~iffer, 1896)
(=Iso-
toma notabilis)
and
Isotomiella minor
(Sch~iffer, 1896 ). Although the shape
of ingested faeces had been lost, due to comminution by buccal parts, the
ingested food is a mixture of different materials, always half-digested and
mixed with bacteria. When no comminution took place in the food bolus, as
was the case in enchyraeid worms, entire faeces were recovered in the guts,
especially the strongly compacted oribatid faeces (Fig. 24 ). This was also ob-
served inside earthworm faeces (Ponge, 1988). Tunnelling of epigeic earth-
worm faeces composed of organic matter by phthiracarid mites
(Rhysotritia
duplicata)
was also observed in the FI layer.
Animal remains on the contrary were commonly encountered, especially in
enchytraeid guts. These were most often tests of testate amoebae. Digestion
of the test of
Trinema
sp. or
Phryganella acropodia (Hertwig
and Lesser, 1874 )
48 J.F. PONGE
Fig. 23. Soil bacteria together with some minute particles in the food bolus of the springtail
Megalothorax minimus. In other respects same as Fig. 22.
Fig. 24.Two oribatid faeces (arrows) in the gut of the enchytraeid worm ('ognettia sphagneto-
rum. In other respects same as Fig. 22.
Hopkinson, 1909, was observed. The case ofP.
acropodia
deserved attention,
because the test of this species is mainly made of aggregated mineral particles.
Careful examination of all clusters of mineral particles found in the intestinal
guts of enchytraeids suggested that they were derived from the disintegration
of tests of this very common species.
INTESTINAL MICROFLORA
Association with bacteria presumed to be living in the intestine was com-
monly observed in all saprophagous groups, except Collembola. Intestinal mi-
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 49
Fig. 25. Associated bacteria (right) near the food bolus (left) in the gut of the oribatid mite
Platynothrus peltifer. L2
layer. Phase contrast. Bar= 50 gm.
croflora might be directly observed as bacterial clouds distinct from the food
bolus (except in Fig. 21 where algal cells were in contact with them), without
any lysis symptom, and was present even in starved animals. These bacteria
were commonly observed in nematoda, rotifera, enchytraeidae, sciarid lar-
vae, oribatid mites (Fig. 25 ) but were never observed in springtails.
SPECIFICITY IN FOOD DIETS
Observation of a great number of soil animals living in the same environ-
ment supported the idea that very few species were specialized feeders and
that the bulk of food resources were consumed without any discrimination.
This held especially true for oligochaeta, i.e., enchytraeid and lumbricid spe-
cies. Nevertheless this view must not be taken as the negation of choice by
soil animals.
The epigeous worm
Dendrobaena octaedra
(Savigny, 1826) was probably
the only lumbricid species present in the sample examined. These animals did
not show any choice in their food diet, as could be judged from their faecal
pellets, and gut contents reflect undiscriminating consumption of the mate-
rial present in the microhabitat occupied by the worm.
The animal species that had been more extensively studied here is the en-
chytreid worm
Cognettia sphagnetorum
( 128 individuals). These animals
showed differences in the ingestion of moss leaves between the three layers
investigated: green leaves were consumed in the Lt layer, dead but uncolon-
ized leaves were ignored in the L2 layer, and leaves colonized by fungi were
consumed in the Ft layer (Ponge 1984, 1985a, 1988). In addition, filamen-
50 J.F. PONGE
tous cyanobacteria ( = blue-green "algae" ), testate amoebae, pollen grains and
resin were more commonly found in the gut of these animals. The absence of
pine needles in the animals present in the L~ layer was probably due to their
early stage of fungal decomposition (especially the strong cuticle which
impeded penetration). This was also the case for the sclerotia of the fungus
Cenococcum geophilum,
which were certainly too hard structures. With these
exceptions all materials available to these animals were actively ingested.
Sciarid larvae (22 individuals) actively consumed moss leaves in the LI
layer, fungal hyphae in the
L2
layer and pine needles in the F~ layer. We can-
not prove that the same sciarid species was involved but this was probably
true, since the individuals seemed to be morphologically identical and be-
longed to the same colonial group.
Collembola were represented by several groups of species, with distinct food
diets. Isotomid species
(Folsomia manolachei,
30 ind.;
Parisotoma notabilis,
24 ind.;
Isotomiella minor,
5 ind.) seemed to be characterized in our litter
sample by their coprophagy. It is difficult to say that this diet was specialized,
since the composition of the pellets so ingested was highly variable, but from
a behavioural point of view, these animals might be classified as specialized
feeders.
Pseudosinella terricola
(8 ind. ) and
Willemia anophthalma
( 8 ind. )
were strictly fungal feeders and the degree of specialization of the second spe-
cies was higher: this animal ingested only the hyaline hyphae of the basidi-
omycete fungus
Hyphodontia.
The other species of Collembola were in too
low numbers to ascertain their food diet.
Oribatid mites, whatever the taxonomic group they belonged to, were the
most specialized animals. Phthiracarids
(Rhysotritia duplicata,
14 ind.;
Phthiracarus sp.,
10 ind. ) ate only pine material (needles and bark), tunnell-
ing within plant tissues. Nevertheless it must be noticed that adults seemed
to have less specialized requirements, since some fungal material (hyphae of
mycorrhizal fungi in the present case) was eaten to a little extent. Oppiids
[Oppiella nova
(Oudemans, 1902), 7 ind.;
Oppia subpectinata
(Oudemans,
1901 ), 9 ind.; undetermined nymphs, 3 ind. ] fed only on fungal hyphae, the
ratio of hyaline versus dematiaceous hyphae varying with the size of the ani-
mals (dematiaceous hyphae of the mycorrhizal
Cenococcum geophilum
needed animals with stronger buccal pieces to break them off). Camisiids
sensu lato
[Platynothrus peltifer
(Koch, 1839), 25 ind.;
Nothrus sylvestris
(Koch, 1839), 5 ind. ] seemed to be specialized in our sample on the mycor-
rhizal
C. geophilum.
It is worthy to note that, although the first species ate
only mycelia in the Ll layer (Ponge, 1984), the second one preferred the my-
corrhizae formed by the same fungus in the Fl layer, ingesting also a small
quantity of some root tissues (Ponge, 1988 ).
If we wanted to classify the different groups investigated according to their
degree of specialization on food resources, we could obtain the following se-
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 51
ries (groups with too few data have been excluded):
Lumbricidae < Enchytraeidae < Sciaridae < Collembola < Oribatida
DISCUSSION
A great deal of work has already been done on the feeding habits of soil
animals. Most conclusive studies concerned only one taxonomic group or even
one single species. The works of Zachariae ( 1985 ) and Bal ( 1970, 1982 ) were
nevertheless closely related to the aim of the present study. Both of these sci-
entists used thin slides of the upper horizons of forest soil to study trophic
relationships that occurred during the decomposition of leaf litter. As was
done in the present study, they attempted to reconstruct a dynamic process
from instantaneous photography. Unfortunately the optic properties of the
hard resins used to embed soil profiles were so questionable that observation
could only be made at the lowest magnification of the light microscope. Other
shortcomings were the absence of fauna in the studied profiles, due both to
the process of desiccation and to the fact that on a given section the probabil-
ity to find animals was very feable. Consequently animal feeding activities
were traced only through their excrements, thus giving no results on digestive
processes.
Enchytraeid worms
In the present study, enchytreid worms were the more thoroughly investi-
gated group (because it was the more abundant at the time of sampling, 129
ind. ), more precisely the acidophilic species
Cognettia sphagnetorum.
In the
aforementioned work of Zachariae (1965), Enchytraeidae were not given a
decisive role in the transformation of beech litter, and their feeding habits
were interpreted as mainly coprophagous. In the work of Bal they were quite
absent (Bal, 1970) or considered as negligible (Bal, 1982 ). This was also the
case in Jacot ( 1939)'s observations on spruce and fir litter. We cannot dis-
pute on these points, but our own experience in temperate forests raises doubts
to the contention'that enchytraeid worms do not play a key role in the com-
minution of leaf litter. The most conclusive work on the feeding habits and
digestion abilities of enchytraeids (also
C. sphagnetorum)
is the study made
by Latter ( 1977 ), Standen and Latter ( 1977 ) and Latter and Howson ( 1978 ).
Latter and co-workers proved, both by field and laboratory experiments and
observation of intestinal guts, that this species thrived on leaf litter
(Rubus,
Eriophorum
or
Calluna),
and that leaf tissues were consumed and finely com-
minuted. Disagreement with our own observations was only with the respec-
tive fate of fungal and plant cell walls. In the present study we did not register
52 J.F. PONGE
any significant change in the appearance of plant cell walls, although crushing
was pronounced. On the contrary, hyaline fungal walls were always partially
digested. Comparison with sciarid larvae, for instance, allowed us to say that
pine cell walls did not seem strongly affected by their passage through enchy-
traeid intestines, apart from their comminution (Ponge, 1988 ). Observation
by light microscopy of the disintegration of cellulosic walls is difficult, due to
their high transparency, but use of phase contrast helped to detect changes in
refringency that might be related to changes in the cristalline structure of cel-
lulose. Observations by light microscopy on the collembolan
ParatuUbergia
callipygos
(B6rner, 1902 ) ( =
Tullbergia callipygos)
suggested that this spe-
cies was able to dissolve cellulose to some extent. This was confirmed by
transmission electron microscopy (Saur and Ponge, 1988). Concerning the
fungal cell walls and their fate, no distinction was made between hyaline and
dematiaceous fungi in Latter's studies, and we showed that only hyaline fun-
gal walls were transformed in the intestine of
Cognettia sphagnetorum.
Ultra-
structural studies on the enchytraeid worm
Fridericia striata (Levinsen,
1884 )
(Toutain et al., 1982), fed on aspen leaves, concluded that plant cell walls
were little affected in its gut (apart from some changes in the microfibrillar
arrangement), contrary to fungal walls that were partly destroyed. Oxalate
crystals that covered the hyphae
of Hyphodontia
did not seem to be dissolved
in the gut of
C. sphagnetorum.
Thus these animals probably do not take a
great part in the cycling of Ca through fungus-animal food chains, in contrast
to what has been claimed by Cromack et al. ( 1977 ) for most soil animals.
Concerning the feeding behaviour of
C. sphagnetorum,
we observed the
tunnelling activity of this species in pine needles, similar to the same behav-
iour inside the cylindrical leaves of the cotton grass (Latter and Howson,
1978). Penetration between bark and wood (phloem part) of dead pine
branches was similarly recorded by these authors on heather woody stems. It
must be noticed that the deposition of faecal pellets at the inside of the tun-
nelled needles was rarely observed, contrary to phthiracarid mites. Exception
is in the L~ layer, where desiccation probably delayed animals escaping from
the needles.
Intestinal microflora was commonly observed, with several morphological
types often occurring together in the same intestine (but in distinctive recta-
meres, Ponge, 1985a).
Oribatid mites
Oribatid mites were the second most abundant group ( 116 ind. ).
Rhysotri-
tia duplicata
( 14 ind. ) and
Phthiracarus sp.
( 10 ind. ) fed on dead plant tis-
sues. They tunnelled pine needles, bark and faeces of epigeous earthworms
and deposited their own faecal pellets inside the so-formed cavities. Tunnell-
ing activity of phthiracarid mites inside litter debris has been recorded time
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 53
and again (Jacot, 1939; KubiEna, 1943, 1953; Handley, 1954; KubiEna, 1955;
Kendrick and Burges, 1962; Zachariae, 1965; Bal, 1970; Babel, 1975; Rusek,
1975; Kubikova and Rusek, 1976; Toutain, 1981; Bal, 1982) and therefore
nothing needs to be added about the importance of these animals in the me-
chanical reduction of plant litter. We observed that pine needles were not
penetrated by these animals until they reached the FI layer, contrary to the
enchytraeid worms, tunnelling by them having been observed as early as the
L1 layer. The question is whether phthiracarid mites were unable to feed on
fresher needles or not, compared to enchyraeid worms. Jacot (1939) indi-
cated that coniferous needles needed to be softened by fungi before any pen-
etration by mites occurred. In the field study made by Kendrick and Burges
( 1962 ) on
Pinus sylvestris
litter, needles were not attacked by oribatid mites
(presumably phthiracarid species) until the "F~" layer, which corresponded
in fact to our L2 layer. The laboratory study by Hayes ( 1963 ) on the conifer-
ous species (including Scots pine) and three phthiracarid species concluded
that needles needed to achieve a particular stage of fungal decomposition in
order to be actively consumed by these animals. Thus our results did not agree
exactly with other studies, although intense fungal penetration of the needles
was considered by these authors as a prerequisite for penetration by phthira-
crid mites. This discrepancy might be partly explained by the fact that our
observations took place on a sample collected in August. This was the time of
intense activity of enchytraeid worms, given the high level of their population
density, probably due to rainy and overcast condition of the weather in the
summer of 1981. Summer was recorded as a period of intense vegetative mul-
tiplication of
Cognettia sphagnetorurn (Springett,
1970). Reproduction of
phthiracarid species
(Rhysotritia duplicata
and
Phthiracarus)
was also effec-
tive at the time of sampling (presence of larval instars of the two species and
eggs of the first), but not at the same rate as Enchytraeidae and they were
probably more evenly distributed over the year: traces of phthiracarid activ-
ity (pellet deposition) were found in a lot of needles that were no longer in-
habited by these animals. Thus we could say that enchytraeid activity was
contemporary and phthiracarid activity rather a remnant of a past one at the
time of sampling. Pine needles that were incorporated into the L layers might
not have been on the ground long enough to be significantly colonized by
phthiracarids. Other species may be classified as mycophagous or "micro-
phytophagous" in the sense of Schuster (in Luxton, 1972). The distinction
between plant feeder species (phthiracarids) and fungal feeders (other spe-
cies, except perhaps
Suctobelba
which seemed to ingest a fluid food) in our
sample corresponded roughly to what was known from the literature on ori-
batid food diets. Nevertheless, some species considered as "panphytopha-
gous" (plant-fungal feeders ) in other sites, were here strictly or mainly fungal
feeders.
Platynothrus peltifer
(25 ind. ) was found to eat exclusively the hy-
phae of the dematiaceous mycorrhizal
Cenococcum geophilum
in the L~ layer
54 J.F. PONGE
(Ponge, 1984 ) and faecal material containing the same fungus in the
L2
layer
(Ponge, 1985a). In the literature, this species was known to eat both plant
and fungal material (Hartenstein, 1962a; Pande and Berthet, 1973; Ander-
son, 1975; Behan-Pelletier and Hill, 1983).
Nothrus sylvestris
(5 ind. ) was
interpreted as a root-fungal feeder (black mycorrhizae of
C. geophilum),
but
mainly browsing the fungal mantle (Ponge, 1988 ). This species was generally
considered as a plant-fungal feeder (Luxton, 1972; Pande and Berthet, 1973;
H~gvar and Kjondal, 1981; Behan-Pelletier and Hill, 1983 ), with plant feed-
ing dominating. Other species, like
Oribatula tibialis
(Nicolet, 1855 ) ( 5 ind. )
and
Nanhermannia nanus
(Nicolet, 1855 ) (5 ind. ) ate a mixture of the two
main mycorhizal fungi present in the studied sample (Ponge, 1988 ), but were
considered as plant-fungal feeders by other authors (Pande and Berthet, 1973;
H~gvar and Kjondal, 1981; Behan-Pelletier and Hill, 1983). Perhaps pine
needles were especially repellent for these species in our study site, neverthe-
less it must be remembered that Pande and Berthet (1973) and Hartenstein
(1962a) worked also in pine stands. We prefer to suggest that the so-called
plant-fungal feeder species favoured fungi which were far in excess of faunal
requirements in the volume under study. Pine needles might perhaps be in-
gested in other times or in other places when preferred a food was not avail-
able, in contrast to phthiracarid mites which seemed to eat only plant mate-
rial. Good agreement with other studies was found only with oppiid species
(Oppia subpectinata,
9 ind.;
Oppiella nova,
7 ind. ), which were considered as
pure fungal feeders (Hartenstein, 1962a; Haq, 1981 ), as in our observations,
but it must be remembered that these small species seemed to choose hyaline
hyphae rather than dematiaceous ones, probably because of the toughness of
the latter.
Food partitioning between co-existing species was studied by Mitchell and
Parkinson (1976). They found that differences in habitats between species
were reflected in their gut contents throughout the year, both qualitatively
and quantitatively. Microcosm experiments of Anderson ( 1978 ) on two re-
lated species demonstrated that at high densities habitat specialization was
influenced by the presence of a competing species and that gut contents were
largely determined by habitats. From our results, several facts may be ascer-
tained. In this small soil volume, we were sure that differences between spe-
cies in habitat and food were determined by environmental constraints and
food preferences and not by differences in food availability. The exception
was when food availability was influenced by micro-environment factors, for
instance an animal physiologically unable to live in the L layers might not
consume living mosses. In the L1 layer, where plant material (mainly pine
needles and moss leaves) and fungal material were co-existing,
Platynothrus
peltifer
was found to eat only dematiaceous hyphae although this species was
known to consume also plant material, including pine needles (see above).
We may suppose either that pine needles and moss leaves were not in a good
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 5 5
decay state or that these fungi (presumably
Cenococcum geophilum)
were
better liked. In the L2 layer, a few millimetres below, the same mite species
was poorly present and apparently ate only the same fungus. In the F1 layer
this mite was absent, although this was the place where
C. geophilum
was well
developed and decaying pine and moss material were present. Thus we may
tentatively suppose that the mite had (at the time of sampling) moved from
the Fl layer and was thus forced to feed in an environment where fungi were
undoubtedly preferred to flesh plant material. Allelopathy (from enchytraeid
worms for instance, with a higher bio-volume) might account for this. In the
FI layer, where most faunal species were present (except
Platynothrus pelti-
fer),
food partitioning was evident between phthiracarid species, which fed
only on plant material, and fungal-feeding species. Some oppiid species were
seen only to ingest hyaline fungi. In this case, buccal anatomy and size of the
animals were probably the main factors responsible for the observed segre-
gation, but food niches for both plant-feeding and fungal-feeding species would
be overlapping.
The fate of the materials ingested by oribatid mites was followed to some
extent. Unfortunately, there is no conclusive study on this problem in the
literature. Plant cell walls seemed to be highly transformed in phthiracarid
species, especially during the transit time in the post-colon, where they lose
their refrigency and sharp contour and became brownish. Ultrastructural
studies would be needed to study these cellulosic and lignocellulosic walls at
the fibrillar level. Fungal walls without melanin were destroyed, except in
Nothrus sylvestris
(Ponge, 1988 ). Oxalate crystals seemed to be dissolved to-
gether with the fungal walls, in contrast to enchytraeid worms. Disintegration
of dematiaceous walls was observed in the gut of
N. sylvestris
and inside faecal
pellets of the other fungal feeding species (Ponge, 1985a), but this was not
observed in any other group.
Presence of an intestinal microflora was commonly observed in
Platynoth-
rus peltifer
and
Rhysotritia duplicata,
where the same morphological strain
seemed to be present in each of these two species, but appeared to be quite
absent in
Nothrus sylvestris
and
Phthiracarus sp.
In the literature, associated
bacteria were reported from numerous oribatid species (Hartenstein, 1962b;
Dinsdale, 1974; Stefaniak and Seniczak, 1983 ) and the latter showed selec-
tion of associated bacteria and actinomycetes was strongly related to the feed-
ing habits of the oribatid species.
Collembola
Feeding habits of springtails have been intensively studied, but several of
our species are uncommon (acidophilic species, Ponge, 1980, 1983 ) and have
not been investigated by other scientists. The present study showed that three
common isotomid species
( Folsomia manolachei, Parisotoma notabilis
and
56 J.F. PONGE
Isotomiella minor)
seemed to be mainly coprophagous, contrasting with my-
cophagous species such as
Willemia anophthalma
and
Pseudosinella terricola.
Comparison with other studies is rather difficult for these species, since faecal
material was mostly overlooked by authors and in the best cases only de-
scribed as "unidentifiable" (Poole, 1959; Gilmore and Raffensperger, 1970 ),
"humus" (Knight and Angel, 1967; Gilmore and Raffensperger, 1970) or
"amorphous" material (Knight and Angel, 1967; B6dvarsson, 1970;
Marshall, 1978; H~gvar and Kjondal, 1981 ). Nevertheless several authors as-
sumed that this material had undergone previous digestion (Poole, 1959;
Knight and Angel, 1967 ). The most important fact in determining the faecal
origin of ingested material was the mixture of distinct strongly decayed ma-
terial (mainly plant and fungal), associated with bacteria dispersed in the
food bolus. Intestinal microflora when present (in other animal groups ) were
always observed as monospecific clouds of bacteria which were never dis-
persed in the food bolus.
Food specialization has been studied by some authors. Most of these works
indicated that coexisting species exhibited differences in resource utilization
but with tremendous overlapping between their respective food spectra.
MacMillan and Healey ( 1971 ) pointed out the fact that some closely related
species (here belonging to the genus
Onychiurus)
did not exhibit significant
differences in their feeding habits, contrary to what was expected. The work
of Bengtsson et al. (1988 ) demonstrated that these animals were influenced
by smell in their choice of food, but their choice was different for animals
reared on agar plates to those reared on soil contaminated with known fungal
species. Hassall et al. ( 1983 ) observed that the vertical migration of one
On-
ychiurus
species into freshly remoistened litter was strongly influenced by mi-
crobial colonization of the decaying leaves. Feeding preferences were mea-
sured by Shaw ( 1988 ) with a great care in the statistical treatment: there was
undoubtedly a constant hierarchy between the different fungal strains to be
tested, but some ranks were not consistent with mortality results, indicating
that the animals did not always feed on the most suitable fungal species. Ver-
hoef et al. (1988) reared two sympatric species on algal, fungal and mixed
diets and compared their growth and fecundity. They found that the most
suitable diets were not necessarily those that were used by field animals. In
laboratory experiments, Ponge and Charpenti6 ( 1981 ) concluded that spores
were always preferred to hyphae in cultural tests of
Pseudosinella alba
fed
with known species of fungi, although spores were rarely found in the gut
contents of field animals. Vegter (1983 ) compared field and cultural obser-
vations and concluded that food specialization between co-existing species
was mainly a reflection of differences in their micro-habitats. Such a conclu-
sion was also supported by the work of Saur and Ponge (1988) where the
proportion of different foods in the gut contents were shown to be dependent
both on season and on vertical distribution of individuals of the same species.
FOOD RESOURCES AND DIETS OF SMALL ANIMALS 57
Our own observations showed in addition that food preferences existed be-
tween species or groups of species living in the same micro-habitat. The fun-
gal content of
Pseudosinella terricola
and
Willemia anophthalma
guts com-
pared to the algal content
ofLepidocyrtus lanuginosus
and to the faecal content
in the three isotomid species was not a consequence of differences in their
micro-habitats. Nevertheless it must not be argued that each Collembola spe-
cies living in the same micro-habitat is specialized in its food habits. Obser-
vations on the three related isotomid species
Folsomia manolachei, Pariso-
toma notabilis
and
Isotomiella minor
showed that no food specialization
existed between them in the studied sample. From the literature and the pres-
ent study we must recognize that no general law currently explains or predicts
soil food webs, apart the minimal evidence that food webs are the conver-
gence point of resources and feeding preferences of animals that are present
in a given place at a given time. Since choices change with the food resources
available to the animals, no model can explain changes in the present state of
our knowledge. Nevertheless it must be remembered that provided the scale
of observation is sufficiently reduced, most significant trends are quite easy
to perceive, although not applicable in samples some distance away.
Observations on the fate of ingested materials were made by a few authors
with the help of transmission electron microscopy (Kilbertus and Vannier,
1979, 1981; Saur and Ponge, 1988 ). They did not correspond to our species,
so unfortunately no comparison could be made with our results. Nevertheless
it must be noticed that soil bacteria may constitute a food for Collembola
(Saur and Ponge, 1988 ), as is probably the case in coprophagous and geopha-
gous species, and that intestinal microflora were never observed in empty guts
(Kilbertus and Vannier, 1981; Saur and Ponge, 1988 ), strengthening the idea
that Collembola do not digest with the help of associated bacteria or
actinomycetes.
Sciarid larvae
The most interesting feature was the succession of dominant materials which
were observed in the gut contents of animals found from the surface to the
deeper regions of the studied profile. Moss leaves (ingested in a green state )
were replaced by fungal hyphae from the LI to the
L2
layer, then by plant
tissues (coming from pine needles) in the
FI
layer. This trend paralleled sim-
ilar features observed in enchytraeid worms (see above), except that pine
needles were ingested by Enchytraeidae at an earlier stage of decomposition
and that consequently there was not a so sharp boundary between the food
diets observed in the three sub-layers. Other differences with enchytraeid
worms were that fungal walls, even when hyaline, were never observed to be
digested by sciarid larvae. On the contrary, sciarid larvae (at least the single
unidentified species which was present in our sample) seemed to be able to
58 J.F. PONGE
digest cellulose, which was not the case for the enchytraeid
Cognettia sphag-
netorum.
Studies on feeding habits of sciarid species are scarce. The obser-
vations of Healey and Russel-Smith 91971 ) and Bal (1970) and the experi-
mental work of Deleporte (1987) established that some species fed actively
on leaf litter. The "small diptera larvae" observed by Zachariae (1965) to
feed on litter between the L and the F layers belonged probably also to the
same family, which we observed to be very common in acid soils, especially
in acid mull or weak moder humus. Further discussion of the present results
is impossible, since the species which was found had not been identified. Only
other work is numerous papers on the damages sciarid larvae cause to mush-
rooms beds.
Earthworms
Food diet of the species
Dendrobaena octaedra
was traced only through its
faeces. This animal did not seem to chose between the available food re-
sources and, apart from comminution, no transformation of plant and fungal
material occurred during the intestinal transit time. Ingestion of leaves by
earthworm species has been recorded many times, but the impact of these
animals on the litter they commonly eat in forests has been very poorly stud-
ied. Rafidison (1982) compared the ultrastructure of the plant material
(beach leaves ) before and after ingestion by the anecic worm
Nicodrilus velox
(Bouch6, 1967) and found that the action of the worm on plant cell walls,
apart from comminution, seemed to be negligible, except in the case of beech
leaves which had been previously decayed by white-rot fungi, similar to our
results on an epigeous species. The same author detected a strong modifica-
tion of the tannin-protein complexes, which was not possible to assess with
our techniques, and it must be noticed that he observed a contact between
beech leaves and soil bacteria, which was only possible in the gut of such a
soil-dwelling species.
Nematoda
The food diet and digestion of some free-living nematodes has been studied
by mean of transmission electron microscopy (Arpin and Kilbertus, 1981;
Saur and Arpin, 1989). These authors accounted for the importance of bac-
teria in the food diet of predatory species belonging to the family Mononchi-
dae and Saur and Arpin (1989) followed the digestive process by comparing
different parts of the same intestine, as in our study. Thus our results were in
fairly good agreement with theirs.
ACKNOWLEDGEMENTS
The author is gratefully indebted to Dr. P.M. Latter (Institute of Terrestrial
Ecology, Merlewood, England) and Dr. J.M. Anderson (University of Exe-
ter, England) for revising of the English language.
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
59
REFERENCES
Anderson, J.M., 1975. Succession, diversity and trophic relationships of some soil animals in
decomposing leaf litter. J. Anim. Ecol., 44: 475-495.
Anderson, J.M., 1978. Competition between two unrelated species of soil Cryptostigmata (Acari)
in experimental microcosms. J. Anim. Ecol., 47: 787-803.
Arpin, P. and Kilbertus, G., 1981. Ultrastructure du contenu digestif et de l'6pith61ium intes-
tinal chez quelques n6matodes pr6dateurs (Mononchida) et bact6riophages. Rev. N6matol.,
4: 131-143.
Babel, U., 1971. Gliederung und Beschreibung des Humusprofils in mitteleurop~ischen W~ild-
ern. Geoderma, 5: 297-324.
Babel, U., 1975. Micromorphology of soil organic matter. In: J.E. Gieseking (Editor), Soil
Components. I. Organic Components. Springer, Berlin, pp. 369-473.
Bal, L., 1970. Morphological investigation in two moder-humus profiles and the role of the soil
fauna in their genesis. Geoderma, 4: 5-36.
Bal, L., 1982. Zoological Ripening of Soils. PUDOC, Wageningen, 365 pp.
Behan-Pelletier, V.M. and Hill, S.B., 1983. Feeding habits of sixteen species of Oribatei (Acari)
from an acid peat bog, Glenamoy, Ireland. Rev. Ecol. Biol. Sol, 20: 221-267.
Bengtsson, G., Erlandsson, A. and Rundgren, S., 1988. Fungal odour attracts soil Collembola.
Soil Biol. Biochem., 20: 25-30.
B6dvarsson, H., 1970. Alimentary studies of seven common soil-inhabiting Collembola of
southern Sweden. Entomol. Scand., 1: 74-80.
Cromack, Jr., K., Sollins, P., Todd, R.D., Crossley, Jr., D.A., Fender, W.M., Fogel, R. and Todd,
A.W., 1977. Soil microorganism-arthropod interactions: fungi as major calcium and sodium
sources. In: W.J. Mattson (Editor), The Role of Arthropods in Forest Ecosystems. Springer,
New York, pp. 78-84.
Deleporte, S., 1987. R61e du Dipt~re Sciaridae
Bradysia confinis (Winn.,
Frey) dans la d6gra-
dation d'une liti6re de feuillus. Rev. Ecol. Biol. Sol, 24: 341-858.
Dinsdale, D., 1974. The digestive activity ofa phthiracarid mite mesenteron. J. Insect Physiol.,
20: 2247-2260.
Esau, K., 1965. Plant Anatomy, 2nd ed. Wiley, New York, 767 pp.
Frankland, J.C., 1974. Importance of phase-contrast microscopy for estimation of total fungal
biomass by the agar-film technique. Soil Biol. Biochem., 6: 409-410.
Gilmore, S.K. and Raffensperger, E.M., 1970. Foods ingested by
Tomocerus
spp. (Collembola,
Entomobryidae), in relation to habitat. Pedobiologia, 10:135-140.
Gochenaur, S.E., 1987. Evidence suggests that grazing regulates ascospore density in soil. My-
cologia, 79: 445-450.
Hhgvar, S. and Kjondal, B.R., 1981. Succession, diversity and feeding habits of microarthro-
pods in decomposing birch leaves. Pedobiologia, 22: 385-408.
Handley, W.R.C., 1954. Mull and mor formation in relation to forest soils. Bull. No. 23, For-
estry Commission, London, 115 pp. + 14 inset plates.
Hanlon, R.D.G., 1981. Influence of grazing by Collembola on the activity of senescent fungal
colonies grown on media of different nutrient concentration. Oikos, 36: 362-367.
Haq, M.A., 1981. Feeding habits of ten species of oribatid mites (Acari: Oribatei) from Mala-
bar, South India. Ind. J. Acarology, 6: 39-50.
Hartenstein, R., 1962a. Soil Oribatei. I. Feeding specificity among forest soil Oribatei. Ann.
Entomol. Soc. Am., 55: 202-206.
Hartenstein, R., 1962b. Soil Oribatei. VI.
Protoribates lophotrichus
(Acarina: Haplozetidae)
and its association with microorganisms. Ann. Entomol. Soc. Am., 55:587-591.
Hassall, M., Visser, S. and Parkinson, D., 1983. Vertical migration of
Onychiurus subtenuis
in
relation to rainfall and microbial activity. In: P. Lebrun et al. (Editors), New Trends in Soil
60 J.F. PONGE
Biology. Proc. 8th Int. Colloquium of Soil Zoology, Louvain-la-Neuve, Belgium, 30/VllI-
2/IX, 1982. Universit6 catholique de Louvain, Louvain-la-Neuve, Belgium, 612 pp.
Hayes, A.J., 1963. Studies on the feeding preferences of some phthiracarid mites (Acari: Ori-
batidae). Entomol. Exp. Appl., 6: 241-256.
Healey, I.N. and Russell-Smith, A., 1971. Abundance and feeding preferences of fly larvae in
two woodland soils. In: Organismes du Sol et Production Primaire. Proc. 4th Colloquium
Pedobiologiae, Dijon, France, 14/1X- 19/IX, 1970. INRA, Paris, pp. 177-191.
Jacot, A.P., 1939. Reduction of spruce and fir litter by minute animals. J. Forest., 37: 858-860.
Kendrick, W.B. and Burges, A., 1962. Biological aspects of the decay of
Pinus sylvestris
leaf
litter. Nova Hedwig., 4: 313-344+ 14 inset plates.
Kilbertus, G. and Vannier, G., 1979. Microbial analysis and weight estimation of feces pro-
duced by four sympatric Colembola species in forest litter. Rev. Ecol. Biol. Sol, 16:169-180.
Kilbertus, G. and Vannier, G., 1981. Relations microflore-microfaune dans la grotte de Sainte-
Catherine (Pyr6n6es ari6geoises ). II. Le r6gime alimentaire de
Tomocerus minor (Lubbock)
et
Tomocerus problematicus
Cassagnau (Insectes Collemboles). Rev. Ecol. Biol. Sol, 18: 319-
338.
Knight, C.B. and Angel, R.A., 1967. A preliminary study of the dietary requirements of
Tomo-
cerus
(Collembola). Am. Midl. Nat., 77: 510-517.
Kretzschmar, A., 1987. Caract6risation microscopique de l'activit6 des lombriciens endoges.
In: N. Fedoroff, L.M. Bresson and M.A. Courty (Editors), Micromorphologie des Sols (Soil
Micromorphology). Proc. 7th Int. Working Meeting on Soil Micromorphology, Paris, France,
VII 1985. AFES, Paris, pp. 325-330.
KubiEna, W., 1943. L'investigation microscopique de l'humus (Die mikroskopische Humusun-
tersuchung). Z. Weltforstwirtsch., 10:387-410.
KubiEna, W.L., 1953. The Soils of Europe. Illustrated Diagnosis and Systematics. CSIC, Madrid
and Thomas Murby and Company, London, 318 pp. + 25 inset plates.
Kubiena, W.L., 1955. Animal activity in soil as a decisive factor in establishment of humus
forms. In: D.K. McE. Kevan (Editor), Soil Zoology, Proc. University of Nottingham Second
Easter School in Agricultural Science, 1955. Butterworths, London, pp. 73-82 + 2 inset plates.
Kubikov& J. and Rusek, J., 1976. Development ofXerothermic Rendzinas. A Study in Ecology
and Soil Microstructure. Academia, Prague, 78 pp. + 16 inset plates.
Latter, P.M., 1977. Decomposition of a moorland litter, in relation to
Marasmius androsaceus
and soil fauna. Pedobiologia, 17: 418-427.
Latter, P.M. and Howson, G., 1978. Studies on the microfauna of blanket bog with particular
reference to Enchytraeidae. I1. Growth and survival of
Cognettia sphagnetorum
on various
substrates. J. Anim. Ecol., 47: 425-448.
Luxton, M., 1972. Studies on the oribatid mites of a Danish beech wood soil. 1. Nutritional
biology. Pedobiologia, 12: 434-463.
Macfadyen, A., 1963. The contribution of the microfauna to total soil metabolism. In:
J. Doeksen and J. Van der Drift (Editors), Soil Organisms. Proc. Colloq. on Soil Fauna, Soil
Microflora and their Relationships, held at Oosterbeek, Netherlands, 10/IZ-16/IX, 1962.
North-Holland, Amsterdam, pp. 3-17.
Marshall, V.G., 1978. Gut content analysis of the Collembolan
Bourletiella hortensis (Fitch)
from a forest nursery. Rev. Ecol. Bio.. Sol, 15: 243-250.
McMillan, J.H. and Healey, I.N., 1971. A quantitative technique for the analysis of the gut
contents ofCollembola. Rev. Ecol. et Biol. Sol, 8: 295-300.
Mitchell, M.J. and Parkinson, D., 1976. Fungal feeding of oribatid mites (Acari: Cryptostig-
mata ) in an aspen woodland soil. Ecology, 57:302-312.
Pande, Y.D. and Berthet, P., 1973. Studies on the food and feeding habits of soil Oribatei in a
black pine plantation. Oecologia (Berlin), 12:413-426.
Ponge, J.F., 1984. Etude 6cologique d'un humus forestier par l'observation d'un petit volume,
FOOD RESOURCES AND DIETS OF SMALL ANIMALS
61
premiers r6sultats. I. La couche
L l
d'un moder sous pin sylvestre. Rev. Ecol. Biol. Sol, 21:
161-187.
Ponge, J.F., 1985a. Etude 6cologique d'un humus forestier par l'observation d'un petit volume.
II. La couche L2 d'un moder sous
Pinus sylvestris.
Pedobiologia, 28:73-114.
Ponge, J.F., 1985b. Utilisation de la micromorphologie pour l'6tude des relations trophiques
dans le sol: la couche L d'un moder hydromorphe sous
Pinus sylvestris
(For~t d'Orl6ans,
France). Bull. Ecol., 16:117-132.
Ponge, J.F., 1988. Etude 6cologique d'un humus forestier par l'observation d'un petit volume.
III. La couche F~ d'un moder sous
Pinus sylvestris.
Pedobiologia, 31: 1-64.
Ponge, J.F., 1990. Ecological study of a forest humus by observing a small volume. IV. Penetra-
tion of litter by mycorrhizal fungi. Eur. J. Forest Pathol., 20: 290-303.
Ponge, J.F., in prep. Succession of organisms during decomposition of needles in a small area
of Scots pine litter.
Ponge, J.F. and Charpenti6, M.J., 1981. Etude des relations microflore-microfaune: exp6riences
sur
Pseudosinella alba (Packard),
Collembole mycophage. Rev. Ecol. Biol. Sol, 18:291-303.
Poole, T.B., 1959. Studies on the food of Collembola in a Douglas fir plantation. Proc. Zool.
Soc. London, 132:71-82.
Rafidison, G.Z., 1982. R61e de la faune dans l'humification: transformations des feuilles de
hfitre par un ver an6cique
(Nicodrilus velox).
Doctorate Thesis, 112 pp., unpublished.
Rusek, J., 1975. Die bodenbildende Funktion von Collembolen und Acarina. Pedobiologia, 15:
299-308.
Saur, E. and Arpin, P., 1989. Ultrastructural analysis of the intestinal contents of
Clarkus pap-
illatus (Nemata:
Mononchina): ecological interest of the survey. Rev. N6matol., 12:413-
422.
Saur, E. and Ponge, J.F., 1988. Alimentary studies on the Collembolan
Paratullbergia callipygos
using transmission electron microscopy. Pedobiologia, 31: 355-379.
Shaw, P.J.A., 1988. A consistent hierarchy in the fungal preferences of the Collembola
Onychiu-
rus armatus.
Pedobiologia, 31: 179-187.
Springett, J.A., 1970. The distribution of life histories of some moorland Enchytraeidae (Oli-
gochaeta). J. Anim. Ecol., 39: 725-737.
Standen, V. and Latter, P.M., 1977. Distribution of a population of
Cognettia sphagnetorum
(Enchytraeidae) in relation to microhabitats in a blanket bog. J. Anim. Ecol., 46:213-229.
Stefaniak, O. and Seniczak, S., 1983. Intestinal microflora in representatives of different feeding
groups of soil moss mites (Acarida, Oribatida). In: P. Lebrun et al. (Editors), New Trends
in Soil Biology. Proc. 8th Int. Colloquium of Soil Zoology, Louvain-la-Neuve, Belgium, 30/
VIII-2/IX, 1982. Universit6 catholique de Louvain, Louvain-la-Neuve, Belgium, pp. 622-
624.
Toutain, F., 1981. Les humus forestiers. Structures et modes de fonctionnement. Rev. Forest.
Fran., 33: 449-477.
Toutain, F., Villemin, G., Albrecht, A. and Reisinger, O., 1982. Etude ultrastructurale des pro-
cessus de biod6gradation. II. Mod61e enchytraeides-liti~re de feuillus. Pedobiologia, 23: 145-
156.
Ulber, B., 1983. Einfluss von
Onychiurus fimatus
Gisin (Collembola, Onychiuridae) und
Fol-
somiafimetaria
(L.) (Collembola, Isotomidae)
aufPythium ultimum
Trow., einen Erreger
des Wurzelbrandes der Zuckerrtibe. In: P. Lebrun et al. (Editors), New Trends in Soil Biol-
ogy. Proc. 8th Int. Colloquium of Soil Zoology, Louvain-la-Neuve, Belgium, 30/VIII-2/IX,
1982. Universit6 catholique de Louvain, Louvain-la-Neuve, Belgium, pp. 261-268.
Vegter, J.J., 1983. Food and habitat specialization in coexisting springtails (Collembola, Ento-
mobryidae). Pedobiologia, 25: 253-262.
Verhoef, H.A., Prast, J.E. and Verweij, R.A., 1988. Relative importance of fungi and algae in
the diet and nitrogen nutrition of
Orchesella cincta
(L.) and
Tomocerus minor
(Lubbock)
(Collembola). Functional Ecol., 2: 195-201.
62
J.F. PONGE
Visser, S., Whittaker, J.B. and Parkinson, D., 1981. Effects of collembolan grazing on nutrient
release and respiration of a leaf litter inhabiting fungus. Soil Biol. Biochem., 13:215-218.
Warnock, A.J., Fitter, A.H. and Usher, M.B., 1982. The influence of a springtail, Folsomia can-
dida (Insecta, Collembola), on the mycorrhizal association of leek, Allium porum, and the
vesicular-arbuscular mycorrhizal endophyte, Glomusfasciculatus. New Phytol., 90: 285-292.
Wolters, V., 1988. Effects ofMesenchytraeus glandulosus (Oligochaeta, Enchytraeidae) on de-
composition processes. Pedobiologia, 32: 387-398.
Zachariae, G., 1965. Spuren tierischer T~tigkeit im Boden des Buchenwaldes. Forstwissensch.
Forsch., 20:68 pp.
