OlKOS 81: 266-278. Copenhagen 1998
Composition and trophic structure of detrital food web in ant nest
mounds of Formica aquilonia and in the surrounding forest soil
Jouni Laakso and Heikki Setala
Laakso. J . and SetaIi, H. 1998. Composition and trophic structure of detrital food
web in ant nest mounds of Fornlica oq~riloniaand in the surrounding forest soil. Oikos 81: 266-278.
Community composition and food web structure of soil decomposer biota in relation
to various habitat properties were compared between upper parts of red wood ant
(Fornlica aqtrilotlia) nest mounds and the adjacent forest soil. For a description of
trophic structure of the decomposer community in the two habitats, soil decomposers
were classified into 14 trophic groups. Classification of the taxa into three habitat
preference categories resulted in a clear division of the fauna into either soil or nest
specialists, relatively few taxa falling between these two groups. A large majority of
the nest specialists belonged to a non-myrmecophilous soil decomposer fauna s o far
largely overlooked in studies on ant-invertebrate associations. Trophic organisation
of the nest mound community differed clearly from that in the soil by having
considerably larger biomass at the base of the food web, and less large predators other than ants - at the top of the web. Contrary to forest soils. the clear dominance
of bacterial feeding microfauna over the fungal feeding microfauna in the nest
mounds suggests that most of the energy passing through the food web is channelled
through a bacterial-based food-web compartment in the nest mounds. Relatively
constant temperature and moisture in the nest surface, continuous energy input by
the ants to the nests, and ant-induced reduction in predation pressure on
macropredators are suggested to be responsible for the development of the typical
decomposer community structure in the nest mounds. Thus. the food-web dynamics
in ant nest mounds represent an interesting case in which the behaviour of an
invertebrate species (i.e. the ant) has a potential to control the development of a
system-level organisation. The high biomass of microbi-detritivorous animals, especially earthworms, in the nest mounds suggests that the activities of the decomposer
fauna may feed back to the structure of nest mound and indirectly alter the
performance of the ant colony.
J. Laakso and H. Setalii, Unic. of Jvriiskylii, Depr of Biological and Encirotznlenral
Science, PO 5o.v 35, FIN-40351 J~rci'sk~A!i.
Finland (jorla@.vzclfi).
Nest building wood ants (Formicidae, Forntica) a r e
k n o w n f o r their large colony size a n d long-lived nest
m o u n d s rich in organic material (Pokarzhevskij 198 1,
Holldobler a n d Wilson 1990). These properties make
the wood a n t nests a suitable habitat not only for
myrmecophilous invertebrates b u t also for a n array
of decomposer animals a n d microbes (see reviews by
Kistner 1982, Holldobler a n d Wilson 1990). Although the high diversity a n d abundance of fauna
Accepted 16 July 1997
Copyright O OlKOS 1998
ISSN 0030-1299
.
Printed in Ireland - all rights reserved
associated with a n t colonies a r e well recognised, t h e
studies are scattered a m o n g various taxonomic a n d
ecological studies of selected genera a n d higher taxa
(Holldobler a n d Wilson 1990: 472). Consequently, attempts t o explain the composition o f a n t nest f a u n a
as a result of ecological processes, such a s a n i m a l
dispersion from the surrounding soil, o r a s a n o u t come of trophic interactions a n d abiotic constraints,
a r e lacking.
There are many theoretical reasons to assume that
the species composition and functional organbation of
the fauna in wood ant nests differ from that in the soil
surrounding the nest. Some of the main community
level constraints, such as productivity and predation
(e.g. Oksanen et al. 1981, Abrams 1993), and abiotic
conditions (Begon et al. 1990) are seemingly different
between the nest mound and the soil, and can thus
provide a reasonable start in search for mechanisms
explaining the community structure in the two habitats.
,
Forest soil is a network of patches where quantity
and quality of basal resources available for heterotrophic organisms, including soil decomposer biota, are
mainly determined by plant production. In this respect
nest building wood ants generate another type of patch
structure in the forest floor. The animal communities in
the nest mounds are more or less dependent on resources the input of which are controlled by the ants,
and therefore these animals can be considered as "primary produceis" for the nest community. This ant-controlled regular flow of basal resources consists of inputs
of fresh litter, prey residues, and honey-dew (up to 230
kg sugar per year) throughout the active season (Skinner 1980). Because these materials are collected from an
area much larger than the area of the nest (radius of a
territory may reach 50 m), the amount of basal resources received by the ant nest community is evidently
much greater than that received by the decomposer
community in the adjacent soil.
Besides productivity, predation pressure is likely to
differ between soil and ant nests. Predatory invertebrates (mainly Coleoptera, Araneae, Formicidae, and
predatory mites) have a potential to control decomposer biota (e.g. Moore et al. 1988, Laakso et al. 1995).
Wood ants play a dual role in the forest floor by
competing with other predators for common prey, and
by feeding upon and interfering with these predators
(e.g. spiders and carabid beetles; see Cherix and Bourne
1980). Thus, the density and species composition of
large invertebrate predators in and close to the ant nest
is potentially different from that of the soil. Theoretically this may lead to indirect, cascading effects down
to the base of the food web (Pimm et al. 1991, Hunter
and Price 1992). That such cascading effects can potentially reach down to decomposer microbes and their
grazers has been suggested by Swift et al. (1979).
Although nest mound materials originate from the
surrounding forest floor, the physico-chemical conditions in the nest mounds are likely to differ from that of
the soil. The nests are built non-randomly in relation to
temperature conditions and vegetation (Laine and
Niemela 1989), and are considerably warmer than other
habitats close to the nest mound (Rosengren et al.
1987). Moreover, the nest structure is not static but is
actively maintained and re-structured by the ants
through continuous input of litter, conifer resin, mineral particles, etc. Consequently, chemical composition,
moisture, and organic matter content are reported to
differ between nest mounds and the adjacent soil
(Pokarzhevskij 1981, Beattie and Culver 1983).
Here we report results of a field study to 1) compare
the structure and trophic organisation of the decomposer community in the uppermost layer of ant nest
mounds with that of the adjacent coniferous forest soil,
and 2) to relate the observed differences to biotic and
abiotic factors potentially controlling the community
level organisation. Due to the high taxonomic diversity
and incomplete knowledge on feeding preferences i f
soil organisms, quantitative analyses on food web patterns that are sensitive to taxonomic resolution (e.g.
Martinez 1991), were not applied. Instead, the taxa in
the nest mounds and in the soil were classified into 14
trophic groups using organism size and feeding preference as criteria, this classification serving as a basis for
the analysis of functional organisation. Several environmental variables were measured to explain the variation
in the species distribution in the ant territories.
Material and methods
Site description
The study site, a 7-ha forest area surrounded by a
clear-cutting and a lake, is located in Konnevesi, central
Finland (62"37'N, 26'20'E). The site is dominated by
mature Norway spruce (Picea abies), silver birch (Betula pendula) and Scots pine (Pinus sylvestris). The area
harbours a dense population (9 ant mounds per
hectare) of wood ants belonging to the Formica rufa
species complex (Formica aquilonia). Due to selective
tree logging, the forest floor receives some sunlight and
has a dense field layer vegetation dominated by Vaccinium myrtillus. The soil type in the area is a wellformed podsol.
Sampling
To investigate the spatial distribution of soil animals in
wood ant territories, 10 out of the 60 nests in the area
were selected for sampling that took place during July
and August in 1993. Medium-sized to large nests
(mean SD diameter I03 24 cm, and height 43 $. 11
cm) without close neighbours were chosen. Nests close
to the edge of the forest area were excluded to avoid
edge effects. The main ant trail structure of the selected
10 nests was mapped and used as basis for selecting
four line transects for sampling (0, 2, l l and 20 m from
the nest centre, 20 m representing the territory edge),
Two of the transects were placed in the vicinity of the
main trails (0.5 m distance), and two transects between
the trails (mean 0.8, 2.9, and 5.9 m from the nearest
trail at 2, 11, and 20 m distances, respectively). Thus,
+
+
for each nest site a total of 13 samples (4 cm thick; 1
sample from the top of nest mound, and 12 from the
surrounding soil) were taken for analysing soil fauna.
Only the uppermost 4 cm of the nest mound was
sampled; according to our experience most of the social& non-integrated animals tend to live in the uppermost layer of the nest (J. Laakso and H. Setala
unpubl.). Sample size for microfauna (Nematoda and
Tardigrada) was 6.3 cm2 (the fauna was extracted using the wet funnel technique used by Sohlenius
(1979)), 10 cm2 for microarthropods (modified Macfadyen high-gradient extraction), 25 cm2 for enchytraeids (wet funnel extraction; O'Connor 1962), and
227 cm2 for macroarthropods (large Tullgren funnel
extraction), and lumbricids (wet extraction; Huhta
and Koskenniemi 1975). Vegetation structure, litter
layer composition, water content (24 h at 80°C), organic matter content (5 h at 550°C), and pH (water)
wereheasured at each sampling point to explain
the variation in the abundance of soil animals. The
composition of vegetation and litter layer structure
was measured at each sampling point as a percent
coverage, separately for the field layer and canopy
layer (sample size 0.39 m2 and 12.6 m2, respectively).
Organic matter content, pH, and earthworm density were determined from half of the line transects
only.
A separate sampling was performed on 27 July
1995, for an estimate of nutrient (N, P, K, Mg,
Ca) content, microbial biomass, and decomposer
activity in the uppermost 4 cm of ant nest mounds,
and in the surrounding soil. The samples (about 500
g in fresh mass) were taken from the surface layer
of five randomly selected nests that were included
in the previous sampling in 1993, and from the soil
(n = 5; 11 m distance from the centre of the nest).
For the estimation of total microbial biomass in
the samples, the substrate-induced respiration method
(SIR; Anderson and Domsch (1978)) was applied.
The samples were homogenised and SIR was measured for 4 subsamples (4 X 3 g organic material,
n = 5). Total nitrogen was determined by the Kjeldahl method, and concentrations of P, Ca, K and
Mg were analysed using plasma emission spectrometry.
Micro- and mesofauna were identified mainly to
species and genera, and larger invertebrates to
families (taxonomic resolution depending primarily on
the developmental stage of a specimen). For the
trophic structure analysis, the taxa were grouped into
13 trophic groups: 1) bacterivores and 2) fungivores,
3) small, 4) medium and 5) large microbi-detritivores,
6) small and 7) large omnivores, 8) micro-, 9) mesoand 10) macrofauna predators, and 11) herbivores.
Due to the high diversity and uncertain nutritional
status of staphylinid beetles (particularly in nest samples), macrofauna-predators were further divided into
two groups; staphylinids as 12) "miscellaneous feeders", and the rest as predators. Similarly, Tardigrada
was categorised as 13) "small miscellaneous feeders".
The trophic grouping was based on feeding preferences obtained from the literature (meso- and macrofauna: Luxton 1972, Persson et al. 1980, Karg 1986,
Werner and Dindal 1987, Walter et al. 1988, Ponge
1991, Siepel and de Ruiter-Dijkman 1993; microfauna: Yeates et al. 1993). Biomasses were estimated
by multiplying individual numbers with actual measured dry masses (10 h at 70°C), or masses acquired
from the literature (Nematoda: Andrassy (1956); microarthropods: Huhta et al. (1986); macroarthropods:
Persson et al. (1980)). A complete list of biomass
parameters and trophic groupings is deposited at
< htpp://www.jyu.fi/bio/jounilaakso/oikos1997/appendixl .doc > .
Statistics
Statistically significant differences in the abundance of
taxonomic and trophic groups of the fauna, and in
the environmental variables between the ant nests and
the soil samples were tested using the Student's t-test
or the Mann-Whitney U-test. The fauna was classified
into nest or soil inhabiting species (hereafter called
"nest preference") by dividing species into three categories based on the ratio of mean density of the taxa
in the two habitats (soillnest > 2: "soil preference",
nest/soil > 2: "nest preference", the rest being "indifferent"). A chi-square test for the three classes was
used to test the null hypothesis that species frequencies in different categories are equal.
To examine the relationship between environmental
variables (plant species exceeding 10% frequency, abiotic variables, F. aquilonia density, and the location
of the sample in the territory) and the fauna, a
Canonical Correspondence Analysis (CCA) was performed using the Canonical Community Ordination
program (CANOCO; Ter Braak 1987). A Monte
Carlo permutation (provided by CANOCO) was used
to test statistically whether the species were significantly related to the environmental variables. Effects
of nest- and trail distance (the "a priori-determined"
variables) were tested separately, whereafter the "forward selection method" provided by CANOCO was
used to select all environmental variables in the analysis that have statistically significant correlations with
the species variables. Finally, the eigenvalues of ordination axes were tested for significant
relations between species and selected environmental variables
relation for the whole data. Since samples for pH,
organic matter content, and earthworm density were
taken only from half of the line transects, two data
sets - one for the whole data set and another for
half of the data - were subjected to the CCA analyses.
Table 1. Coverages (%, mean f SE) of dominant types of litter, and field and canopy layer vegetation at the soil sampling sites
(1 18 samples), and at the nest sampling sites (10 samples). Statistical differences between the means are indicated by asterisks
(Student's t-test; ns: P > 0.05, *: P = 0.05-0.01, **: P = 0.01-0.001, **: P < 0.001).
Litter
Picea abies
Betula pubescens/pendula
Pinus sylvestris
Hay litter
Field layer vegetation
Vaccinium myrtillus
Deschampsia flexuosa
Calamagrostis arundinacea
Gymnocarpium dryopteris
Pteridium aquilinum
Canopy layer vegetation
Picea abies
Betula pubescens/pendula
Pinus sylwstris
Sorbus auntparia
Alnus incana
.
Populus tremula
Soil
Nest
3.9
24.4
1.1
3.4
Total 33.1
+0.8
z1.8
k0.2
0.6
+2.1
47.9
23.7
9.3
0.3
81.2
- 10.7
9.2
3.9
z0.3
k5.7
+2.5
+0.8
z2.3
k1.4
k1.1
+2.2
3.5
2.0
6.3
0.0
0.4
13.0
+ 1.2
+ 2.0
k0.3
k3.11
***
z+2.5
1.6
0.9
17.0
12.0
10.5
1.1
1.1
0.5
45.1
k 10.3
+ 5.8
24.3
k0.7
k1.0
- 0.5
f9.0
ns
ns
ns
ns
ns
ns
ns
P
+
26.8
6.2
12.8
5.9
2.4
Total 66.6
p
16.4
16.0
5O
.
1.3
0.2
0.4
Total 39.4
+_
f0.3
+0.1
z0.3
f2.3
+
+
**
ns
ns
+
***
***
***
ns
+ 2.0
*
***
70.0
ns
+
Animal community structure in relation to environmental variables
Results
Habitat characteristics
Composition of litter, and composition of field layer
vegetation differed between the nests and the soil
(Table 1). The nest mounds were topped with a thin
(0.5- 1.5 cm), dry layer of fresh litter, underneath which
there was a moist layer (2-10) of more decomposed
litter. Significant amounts of conifer resin particles
(diameter <0.5 cm) and earthworm faeces were found
in the surface layer of the nest mounds. pH, dry matter
content, and organic matter content were all significantly higher in the nest material than in the soil
organic layer (Table 2). Amounts of N, P, K and M g
per unit dry matter did not differ between the soil and
the nest materials. However, concentration of C a was
37 % higher in the nest material than in the soil. When
nutrient content was examined in relation t o organic
matter content, nitrogen and phosphorus concentrations were higher in the soil than in the nests (Table 2).
A total of 180 taxa and developmental stages o f fauna
were identified, 127 of which were found i n the nests
(average 50 groups per sample), and 168 were present in
the soil (average 55 groups per sample). A s C C A
analyses with the smaller data set (see methods) gave
essentially the same results for the nest-soil comparisons a s analyses with the large data set containing fewer
environmental variables, only the results obtained from
the smaller data set are vresented. C C A analvsis with
Monte Carlo permutation showed that distance from
the nest and trails (the a priori-determined variables)
alone can significantly explain variation in the animal
densities (Table 3; significance tests for the axes). When
data analysis is performed by selecting only the most
significant environmental variables out of the 38 measured environmental variables ("forward selection"
method at P < 0.05 level), other variables, being however correlated with nest and trail distances also be-
Table 2. Characteristics of soil and ant nest materials (mean +_ SE). dm = dry matter content (%), om = organic matter content
(O/O).Total nutrient concentrations are g/kg. Statistical differences between means are indicated by asterisks (Student's t-test);
n = soil/nest sample size. For explanation of the asterisks see Table 1.
p
-
pH (water)
Soil
Nest
1-test
n
4.69
+0.06
dm
om
29 + 1 50+3
5.42
kO.08
54+4
86+2
***
***
***
60110
60110
60110
N dm
N om
12.4
1.9
10.6
k0.6
21.2
+1.3
12.2
+0.6
515
515
*
P dm
P om
K dm
K om
Mg dm
Mg dm
Ca dm
Ca om
1.06
1.9
0.93
k0.12 k0.2 k0.12
0.91
1.0
1.08
k0.05 k0.0 k0.06
ns
*
ns
515
515
515
1.7
k0.3
1.2
k0.1
ns
515
0.62
k0.07
0.77
k0.04
ns
515
1.3
k0.4
0.9
k0.1
ns
515
3.65
k0.72
5.80
f0.34
6.5
+l
6.7
k0.5
ns
515
*
515
Table 3. A biplot of the relationship between environmental variables and species composition of the samples in canonical
correspondence analysis (CCA): eigenvalues for the three ordination axes, percentage of variation explained by the a priori- or
forward selected environmental variables (axis I), and test of significance (Monte Carlo permutation) for the first axis, and all
axes with 99 permutations that gives a minimum confidence level of P = 0.01.
Eigenvalue,
explained,
Permutation,
Permutation,
overall test
%
axis 1
axis 2
axis 3
axis I
axis 1
CCA for the a prioriselected variables (nestand trail distance)
CCA with the forward-selected
variables (nest distance, dry and
organic matter content, pH, Picea
coverage
0.263
0.025
0.420
91.2
0.515
0.079
0.046
F-ratio 8.72, P = 0.01
F-ratio 4.84, P = 0.01
came included (Table 3 and Fig. 1 for the species-environment biplot). Community composition of soil fauna
was significantly correlated with nest distance, Picea
canopy coverage, soil pH, organic matter and water
content (Table 3). Most of the variation explained by
the environmental variables was between the nests and
the surrounding soil (Fig. 1; axis 1 separates nests from
surrounding soil and has the highest eigenvalue: Table
3; ordination results with forward selected variables)
and consequently these two habitat types can be compared without loosing much information.
Characteristic taxa in the nests and in the soil
Classification of the taxa into three "preference categories" resulted in a clear division of the fauna into
either soil or nest specialists, relatively few taxa falling
between these two groups (Fig. 2; chi-square test for
random grouping: P < 0.0001). See ,< htpp://www.
jyu.fi/bio/jouni~laakso/oikosl997/appendixl
.doc > for
classification of each taxa.
Microfauna
Ant nests were dominated by one or two taxa of
bacterial (family Rhabditidae and genus Plectus) and
fungal feeding (two Aphelenchoides species) nematodes,
while the composition of the Nematoda community in
the soil was more diverse and more evenly distributed
among the taxa (bacterivorous Plecrus spp., Rhabditidae, Teratocephalus spp. and Acrobeloides spp., and of
the fungal feeders two Aphelenchoides species, Tylencholaimus spp. and Malenchzrs spp.). Densities of both
bacterial feeders and fungal feeders were higher in the
nests than in the soil, whereas the predatory mononchids (genus Prionchulus) were more numerous in the
soil. he mononchids were the dominant microfaunal
predators in the soil, but in the nest mounds the
mononchids represented only 1.S% of the microfauna
predator biomass. Tardigrada showed similar patterns
as nematodes, their density being 4.6 times higher in the
nests than in the soil.
74.1
F-ratio 18.66, P = 0.01
F-ratio 5.61, P = 0.01
Enchytraeids and earthworms
The enchytraeid Cognettia sphagnetorum was the most
numerous mesofaunal species in the forest soil, but it
was almost absent in the nests. Earthworms were abundant in the nests: an average of 128 (0.95 g d.m.) and
705 (6.87 g d.m.) earthworms per m2 were found in the
soil and in the nests, respectively. Dendrodrilus rubidus
was found almost exclusively in the nests, whereas
~endrobaenaoctaedra inhabited both the nests and the
soil.
Collembola and Acari
In the forest soil collembolans and mites were equally
numerous with several abundant species (see t h t p p : / j
www.jyu.fi / bio / jouni-laakso / oikos1997 / appendixl.
doc > for a complete listing). In the nests, however,
several mite species (belonging to Oribatida, Uropodina
and Gamasina groups) were abundant and only two
collembolan species (Friesea mirabilis and especially
Lepidocyrtus cyaneus) reached moderate densities. Typical "nest specialists" in Oribatida were Brachychtoniidae, Heminothrus peltifer, Ramusella clavipectinata
(Ramusella instead of other Oppioidea species that were
abundant in the surrounding soil), Pergalumna nervosa
and Carabodes subarcticus.
Insects
The nests harboured a ten times more abundant insect
fauna (l1 687 m-2) than the soil (1191 m-2). Typical
insect taxa in the nests were of Ptilidae, Staphylinidae
and Coleoptera larvae (type 1, classified as predaceous)
and Diptera larvae (Nematocera). In soil, Protura, Heteroptera, Coccoidea and small Diptera larvae (type 1 )
were commonly found.
Food-web architecture
The food-web configuration of the decomposer community in the soil and in the nests is presented in Fig. 3.
Dominant species in terms of biomass within each
trophic group and habitat are listed in Table 4. The
OIKOS 8 1 2 (1998)
NESTDIST
AXIS
t--t---t
I
Fig. 1. Distribution of soil fauna in the ant nest mounds and in the surrounding forest soil in a biplot with respect to the five
significant environmental variables (indicated as arrows; nestdist = distance from the nest; pH = substrate pH; drymatt = dry
matter content; om-cont = organic matter content; pi-cov = Picea canopy coverage), using CCA. = nest samples; = 2 m
distance from nest, and 50 cm distance from nearest trail; 0 = 2 m, between trails; W = 11 m, 50 cm from trail; = 11 m,
between trails; A = 20 m, 50 cm from trail; V = 20 m, between trails.
*
basal resource for the soil food web is mainly composed
of litter, humus, and roots. The surface layer of the ant
nest differs clearly from that of the soil, the dominant
basal resources including needle litter, unquantified
amounts of prey residues, and conifer resin. The first
trophic links in both habitats are the ones between dead
organic matter (DOM) and microbes, and between
DOM and microbi-detritivorous fauna. Fungi and bacteria are the dominant groups exploiting the DOM both
in the nests and in the soil. The total microbial biomassC was 3 times higher in the nests than in the soil (Table
5). Similarly, biomass of the fauna that feed upon
detritus (mostly earthworms) was approximately 4-fold
in the nest mounds as compared to that in the soil.
A large majority (68%) of animal biomass in the nests
(totalling 10.0 g d.m./m2) was composed of large microbi-detritivores (earthworms), that formed the second
trophic link together with the two smaller microbi-detritivore groups and microbivorous nematodes. The total
biomass of small and medium-sized microbi-detritivores
was two times higher in the nests than in the soil.
Contrasting to the nests, animal biomass (2.6 g d.m./m2)
in the soil was more equally distributed among large
(36.5% of the total biomass) and medium-sized (37.9%)
microbi-detritivores, macrofauna predators (7.8%) and
herbivores (5.7%). Biomass of bacterivorous nematodes
was 10.0 times higher in the nests than in the soil,
whereas fungivorous nematodes were 4.4 times less
abundant in the nests than in soil (the ratio of bacterial
to fungal feeders being 0.44 and 18.9 in the soil and in
nests, respectively).
Quantitative differences in the food web configuration between the nest and the soil were found also high
up in the food web. The biomass of macrofauna predators in the nest mounds was only 47.3% of that in the
soil (note that staphylinid beetles are excluded from the
group). The biomass of mesofauna predators was 3.2
times'higher in the nests than in the soil (the ratio of
mesofauna predators to their potential prey - small
and medium-sized microbi-detritivores - was 0.051 and
0.089 in the soil and .the nests, respectively). Microfauna predators were 9.1 times more abundant in the
nests than in the soil; the ratio of microfauna predators
to nematodes - the potential prey for microfauna being 1.37 in the soil and 3.97 in the nests.
Staphylinid beetles, of which some species are predators and some microbial/detrital feeders and social parasites (Kistner 1982), were a significant component of
the nest fauna (biomass 8.7 times larger in the nests
than in the soil). Small miscellaneous feeders
(Tardigrada) and omnivores had only a small contribution to the total faunal biomass in both habitats.
When the habitat-preference classification of the taxa
is studied in relation to the biomass of the fauna, it
becomes apparent that the functional organisation of
the nest fauna is dominated by habitat specialists
(97.4% of the nest fauna, including the earthworms),
whereas in the soil habitat specialists were less important group (50.3%).
Discussion
Habitat characteristics and species composition
The uppermost surface layer of the ant nest mound
harboured an abundant and functionally specialised
decomposer community that clearly differed from that
of the surrounding soil. This is not surprising since the
many environmental factors known to affect the abundance and distribution of soil fauna (see e.g. Anderson
1977) differed strongly between the ant nests and the
soil. For example, the high temperature and' constant
moisture in the nest mounds (Rosengren et al. 1987, J.
Laakso and H. Setala unpubl.) evidently impact the
development of the community composition of the
decomposer food web. According to Rosengren et al.
(1987) the mean temperature in the nest centre (30-60
cm from the top) is typically 25-30°C during the active
period for the ants. The uppermost layers are cooler about 22°C from May to September - yet significantly
warmer than the surrounding soil (ca 12°C at the study
site during the summer; H. Setala and J. Laakso unpub].). The high temperature in the nest mound can
result from microbial activity in the decomposing ant
nest materials (Coenen-Stass 1980), or is an outcome of
thermoregulatory activities of the ants (Rosengren et al.
1987) in the nest centre. We hypothesise that the constant moisture in the nest surface results from this
biotic activity: the warm, uplifting air produced in the
nest centre contains water vapour that condenses in the
cooler surface layer of the nest. This, together with a
continuous and abundant input of resources, such as
litter and prey residues, is responsible for the distinct
and highly suitable conditions for many decomposer
microbes and fauna to live in.
The distinctness of the faunal composition in the two
habitats is further demonstrated by the clear classification of the fauna into habitat-preference categories:
both habitats harboured large amounts of specialists,
whereas generalists inhabiting both habitats were
scarce. The abundance of nest specialists makes the
nests unproportionally important for species richness of
the forest floor; nest mounds, covering an area less than
0.1% of the whole study site, harbour approximately
36% of the taxa that are scarce in the adjacent soil (see
Fig. 2). It is, however, worth noticing that a large part
of the taxa named here as "nest specialists" (such as
Dendrodrilus rubidus; Stop-Bijwitz (1969)) are common
inhabitants of more fertile soils than is the one at our
study area, and that soil sampling in this study did not
include other special habitats, such as decaying tree
stumps, mushrooms and carcasses.
SOIL
INDIFFERENT
NEST
Forest soils can be characterised as relatively stable
Fig. 2. Frequency of soil animal taxa in the F. rufa territories
classified as soil specialists, indifferent species, or ant nest habitats for soil biota because the turnover times of
specialists. The classification is done by dividing animal spe- trees, and particularly that of humus, are vastly longer
ciesltaxa into categories based on the ratio of mean density of than that of the fauna (Bengtsson 1994). Nest mounds
the taxa in the ant nest mounds and in the adjacent soil
(soil/nest > 2: "soil preference"; nest/soil > 2: "nest prefer- of wood ants may well be even more stable habitats
than forest soils because of the active regulation of
.
ence"; the rest: "indifferent").
(a)
FOOD WEB OF THE SOIL ORGANIC LAYER
Total biomass 2.6 g /m2
MC&-Detntl-
-D. H h i d ~ 9 %
FOOD WEB OF THE ANT NEST SURFACE
Total biomass 10.0 g /m2 + F. aquilonia ants (>>l0 g/m3
Large Microbri-DegitiYms:
E w t h w m s 6.87 g / &a
D. nrbieim 638 952
D. o c t a e h 32 %
Micd-Wt-
FUNGI and BACl'E.UA (4.92 mg C,
/ g dw)
Fig. 3. Trophic organrsation of decomposer food web in the so11 and m the upper surface layer of ant nest mounds. The area
of the boxes 1s proportronal to the mean b~omass(dry mass) of a trophic group in the habitats. BV = bacter~vorousmicrofauna
(excluding Protozoa), FV = fungivorous mtcrofauna, MDV = small mtcrobi-detnt~vorousfauna. A question mark followed by ap
arrow, denotes unknown feedrng relat~onshtps
Table 4. Biomass (d.m. mg/m2) of the fauna in each trophic group, and proportion (%) from total animal biomass in the ant nest
and in the soil. The dominant taxa (taxa having >5% proportion of group biomass in soil or the nests are included) within a
trophic group in soil and the nests (percentage calculated from a trophic group biomass). See Table 1 for explanation of the
asterisks denoting statistical differences between the means.
Soil
YO
67.2
18.6
13.8
9.44
8.66
150
51.6
14.3
10.6
7.2
6.6
5.7
1.0 I O - ~
4.74
< 1.0 X I O - ~
0.44
26.4
32.6
<O.l
14.5
<0.1
1.4
81.1
0.3
3.24
1.14
0.8 1
0.75
0.69
0.44
Total 7.69
42.2
14.8
10.5
9.8
8.9
5.8
0.3
7.7 I
59.4
0.06
0.04
3.39
4.07
75.7
10.2
78.5
0.1
0.1
4.5
5.4
0.8
17.0
0.49
0.08
17.6
96.8
2.8
0.5
0.7
< 1.0 X I O - ~
2.83
1.18
4.01
<0.1
70.7
29.3
<0.1
Herbivores
Curculionidae
Coccoidea
Lygaeidae
Heteroptera juv.
Lepidoptera juv.
Total
Bacterivores
Plectus spp.
Rhabditidae
Teratocephalus spp.
Acrobeloides spp.
Plecrus sp. 1
Cervidellus spp.
Fungivores
Tylencholaimus spp.
Aphelenchoides sp. 1
Aphelenchoides sp. 2
Total
Microbi-detritivores, large
Dendrobaena octaedra
Dendrodrilus rubidus
868
86.6
955
Total
Microbi-detritivores, medium size
Cognettia sphagnetorum
534
Nothrus silvesrris
141
Nanhermannia sellnicki
61.1
Heminothrus peltifer
56.2
Carabodes subarcticus
4.37
Pergalumna nervosa
2.90
Total 992
Microbi-detritivores, small
Isotomiella minor
14.0
Isdoma hiemalis
12.9
Oppiella nova
13.0
Conchogneta traegardhi
11.9
Folsomia quadrioculata
11.8
Tectocepheus velatus
8.76
Suctobelbidae
7.04
Nothridae juv. small
6.96
Folsomia jimetaria
6.12
Porobelba spinosa
0.94
Belbidae spp.
0.84
Ramusella clavipectinata
0.05
Total 117
Macrofauna predators
Araneae
101
Carabidae
67.7
Coleoptera juv. type 1
25.7
Total 205
Mesofauna predators
Gamasina juv.
29.9
Veigaia nemorensis
10.1
Pergamasus brevicornis
5.06
Gamasina spp.
4.17
Rhagididae
3.61
Sejus toecatus
0.21
Total 56.9
90.9
9.1
36.5
Nest
%
2195
4669
6865
32.0
68.0
68.4
53.9
14.2
6.2
5.7
0.4
0.3
37.9
31.4
5.69
25.5
712
272
403
1900
1.7
0.3
1.3
37.5
14.3
21.2
18.9
12.0
11.0
11.0
10.1
10.0
7.5
6.0
5.9
5.2
0.8
0.7
<0.1
4.5
0.80
1.99
0.93
0.43
0.72
2.72
0.48
39.5
0.30
6.44
15.6
26.1
116
0.7
1.7
0.8
0.4
0.6
2.4
0.4
34.1
0.3
5.6
13.5
22.6
1.2
49.1
33.0
12.5
7.8
31.9
< 1.0 X I O - ~
64.3
97.1
32.9
<0.1
66.2
I .O
52.6
17.8
8.9
7.3
6.3
0.4
2.2
163
0.86
< 1.0 X low'
2.51
0.33
12.7
180
90.7
0.5
<0.1
1.4
0.2
7.1
1.8
,
U-test
Table 4 (continued)
Soil
Microfauna predators
Mononchidae
Trachyfes spp
Nest
100
10.0 X lo3
%
U-test
11.9
5.99
4.20
3.58
3.20
2.93
0.73
0.54
Total 34.7
Parazercon radiatus
Uropodina juv
Urodiaspis tecta
Dinychus perforatus
Oodinynchus polyctenaphila
Oplitis paradoxa
Miscellaneous feeders, small
Tardigrada
1.52
Total 1.52
Miscellaneous feeders, large
Staphylinidae
52.0
Total 52.0
Omnivores, large
Pulmonata type 2 (without shell)
Pulmonata type 1 (with shell)
Omnivores, small
19.8
16.9
Total 36.7
8.90
3.43
0.25
Total 12.9
Dorylaimus
Rotylenchus
Friesea mirabifis
,
YO
Total 2.62 X 103
Animal biomass,
abiotic conditions in the nest, and due to the continuous energy supply by the ants. As a result of these
activities the small-scale habitat heterogeneity in the
nest surface is also reduced. The two factors, environmental stability and homogeneity, are commonly regarded to increase the strength of biotic interactions
(e.g. Begon et al. 1990) which can therefore be assumed
to tk an important factor in structuring the species
assemblages in ant nest mounds. Indeed, the lack of the
enchytraeid Cognettia sphagnetorum - the most abundant species in the food web of the forest soil - and the
massive increase of earthworms in the nests may results
from competition between these faunas. Enchytraeids
and earthworms use similar resources (Persson et al.
1980), and have been reported to show competitive
interaction with each other (Persson et al. 1996). However, the two species do not seem to compete under low
pH conditions, whereas in high pH earthworms may
practically exclude C . sphagnetorum (Persson et al.
1996). Intense predation is also a plausible explanation
for the absence of C. sphagnetorum due to the extremely
high amount of ants and microarthropods that can feed
on the enchytraeids. Further, it should be noted that
the absence of C. sphagnetorum in the nests cannot be
explained by unsuitable abiotic conditions or lack of
food resources in the nests: in our two-month experiment (H. Setala and J. Laakso unpubl.) with individuals of C . sphagnetorum enclosed in 27-km mesh-bags
containing defaunated substrate, neither the substrate
quality (soil organic matter vs nest-mound litter) nor
the abiotic conditions (the litter-bags incubated in the
humus layer of the soil or in the moist surface material
of an ant nest) had a negative influence on the growth
rate of Cognettia. As pointed out by Rahel (1990)
stable communities with predictable environmental conditions are the best candidates to study intense biological interactions (e.g. for examining competition theory).
We conclude that ant nests would be excellent candidates for such studies: besides predictable abiotic or
biotic conditions, nest mounds are distinct habitats with
sharp boundaries allowing easy manipulation of both
the biotic and abiotic environment for experimentation.
Table 5. Microbial biomass C (mg C,,,/g dry mass), basal respiration at 22OC (pg C g-' dry mass h-'), and metabolic quotient
(g CO,-C/g C,!,) in the soil and in the surface layer of ant nests (mean SE). See Table 2 for explanation of the asterisks
denoting statlst~caldifferences between the means (Student's t-test, n = 5).
+
--
Soil
Nest
P
Microbial biomass
Basal respiration
Metabolic quotient
1.72 +_ 0.3
4.92 f 0.33
37.98 + 9.06
84.68 + 3.59
0.0214 + 0.002
0.0174 f0.001
ns
***
**
Therefore these "hot spots" of biological activity can
be seen as a kind of "natural microcosms" providing an
unrestricted opportunity for the organisms to freely
disperse into and out of their habitat.
Food-web organisation
The most profound difference in the functional organisation between the nest and the soil decomposer community was the large biomass concentrated at the lower
trophic positions (microbes, microbivores and detritivores) in the nest mounds. With some exceptions, the
increased productivity at the lower trophic levels should
reflect in increased biomass of the upper trophic levels
if they are not intensively regulated from above (e.g.
Oksanen et al. 1981, Abrams 1993). That this was not
the case for predatory arthropods (e.g. spiders and
carabid beetles), other than ants, can be readily explained by the capability of ants to deter or predate
upon these arthropods (Cherix and Bourne 1980). Besides providing food source to the ants, the lack of
large generalist arthropod predators reduces the risk of
ant developmental stages of being predated by these
predators (Holldobler and Wilson 1990). Further, it is
unlikely that ants themselves can directly contribute to
the top-down regulation of the total biomass of microbivore and detritivore populations; even weak predatory interactions under the extremely high density of
ants should effectively reduce or exclude these populations in the nests. Thus, the large biomass of mediumsize and large microbi-detritivores in the nests can be
explainable by abundant basal resources, and weak (or
non-uniform) predatory pressure on this fauna, both of
which are determined by the behaviour of the ants.
Moore and Hunt (1988) suggested that resources in
decomposer food webs are compartmentalised into "energy channels" originating from detritus, bacteria,
fungi, and plant roots. In coniferous forest soils the
majority of microbial biomass is in fungal mycelia
(Persson et al. 1980), which is mainly responsible for
the energy transfer in these habitats (Ingham et al.
1989). It is, however, reasonable to assume that in ant
nests the energy flow starting from decomposing litter
material is channelled mainly via the bacterial-based
food-web compartment. That nematodes can be
classified into fungal and bacterial feeders can be used
to indicate the relative abundance of bacteria and fungi
(Twinn 1974, Ingham et al. 1989), and thus to indirectly
describe the relative significance of the two energy
channels. In our data, the ratio of bacterial to fungal
feeding nematodes in the soil was in favour of fungivores, whereas in the nests the ratio was strongly biased
to bacterial feeders'. Our presumption on the dominance
of bacteria in the nest mounds is further supported by
the high biomass and activity of earthworms (Edwards
and Bohlen 1996, Persson et al. 1996), high pH and Ca
content (Alexander 1977), and the low amount of plant
roots that support mycorrhizal fungi, all of which are
reported to increase the bacteria:fungi ratio in soils.
The high and relatively constant temperature inside
the Formica nest mounds throughout the active season
(Rosengren et al. 1987) is likely to increase the turnover
rates of microbes and their consumers. Therefore the
difference in the secondary production between the nest
and soil decomposer communities must be considerably
greater than the measured biomasses and basal respiration rates (the latter obtained by incubating the nest
and soil samples at a constant temperature) would
suggest. This would further emphasise the position of
ant nests as "hot spots" for decomposer communities in
forest soils.
Function of the decomposer food web and ant-nest
performance
As the behaviour of ants (e.g. choice of prey, nest
building materials and regulation of temperature) can
actively,modify the structure and function of the community in the nest mounds, it is possible that this
behaviour can indirectly reflect on ant performance and
consequently act as selective, community/ecosystemlevel feed back mechanism which modifies ant behaviour. Creation of highly favourable conditions for
decomposer activity may increase costs for maintaining
the physical structure of the nest mound. Further, the
high energy input by the ants can favour not only the
growth of heterotrophic decomposer microbes, but also
the development of microbes to be facultatively
pathogenous for the ants (Gillot 1980: 649). Another
question is whether the maintenance of a certain kind
of trophic organisation or a composition of decomposer species could benefit the ants. For example, the
large earthworm biomass in the nest surface is a potential source of nutrition for the ants - yet this fauna is
untouched by the ants. An explanation for this curious
phenomenon is that the earthworms can secrete ant
repelling mucus, and/or that the behavioural traits of
the ants have been selected for an active avoidance
because of the benefits the worms provide when not
eaten are greater than the benefits they provide as a
food source (Laakso and Setala 1997). The potential
benefits include feeding on fungi and increase of bacteria to fungi ratio (Edwards and Bohlen 1996, Persson et
al. 1996) by the earthworms which may prevent the nest
surface from becoming overgrown by moulds and fungal mycelia. Excessive hyphal mats - sometimes occurring in old, almost abandoned nest mounds (J. Laakso
and H. Setila unpubl.) - bind litter particles tightly
together, potentially hindering the ants to re-structure
the nest mound. This, in turn, may prevent the ants
from efficiently controlling temperature and moisture
conditions in the nest. Thus, the unhostile behaviour of
OIKOS 81:2 (1998)
ants against earthworms, together with predation o r
interference against other fauna feeding o n earthworms,
m a y modify the food web organisation for the ants'
benefit.
Acknowledgements - We thank the Jyvaskyla soil research
group and Jouni Taskinen for improving the manuscript. Petri
Ahlroth, Jari Haimi, Veikko Huhta, Ritva Niemi and Pekka
Lehtinen gave invaluable help with the daunting task of
identifying arthropods. We will remember with warmth the
cheerful moments spent at Konnevesi Research Station. The
study was initially sponsored by KELA (grant 080667-139s)
and later by the Academy of Finland.
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