The Role of Wood Ants (Formica rufa group) in Carbon and Nutrient Dynamics of a Boreal Norway Spruce Forest Ecosystem

Abstract

Wood ants (Formica rufa group) are regarded as keystone species in boreal and mountain forests of Europe and Asia by their effect on ecosystem carbon (C) and nutrient pools and fluxes. To quantify the impact of their activity on boreal forest ecosystems, C, nitrogen (N), phosphorus (P), potassium (K) and calcium (Ca) pools and fluxes in wood ant nests (WAN), and soil were assessed along a 5-, 30-, 60-, and 100-year-old Norway spruce (Picea abies L. Karsten) dominated successional gradient in eastern Finland. Amounts of C and nutrients in WAN increased with stand age, but contained less than 1% of total C and nutrient pools in these stands. The CO2-efflux from nests was also insignificant, as compared to CO2-efflux from the forest floor. Annually, the amount of C brought by wood ants into their nests as honeydew, prey and nest-building materials ranged from 2.7 to 49.3 kg ha−1 C, but this is only 0.1–0.7% of the combined net primary production of trees and understorey in boreal forests. The difference between wood ant nest C inputs and outputs was very small in the younger-aged stands, and increased in the older stands. Carbon accumulation rates in nests over a 100 year period are estimated to be less than 10 kg ha−1 a−1. In contrast to C, annual inputs of N, P, and K are larger compared to wood ant nest nutrient pool size, ranging from 3 to 6% of the annual tree stand and understorey uptake. This indicates a more rapid turnover and transport of N, P, and K out of WAN, and suggests that wood ants increase the cycling rate of these nutrients in boreal forests.

Full text

The Role of Wood Ants (Formica
rufa group) in Carbon and Nutrient
Dynamics of a Boreal Norway Spruce
Forest Ecosystem
Leena Fine
´r,
1
* Martin F. Jurgensen,
2
Timo Domisch,
1
Jouni Kilpela
¨inen,
1
Seppo Neuvonen,
1
Pekka Punttila,
3
Anita C. Risch,
4
Mizue Ohashi,
5
and
Pekka Niemela
¨
6
1
Finnish Forest Research Institute, P. O. Box 68, 80101 Joensuu, Finland;
2
School of Forest Resources and Environmental Science,
Michigan Technological University, Houghton, Michigan 49931, USA;
3
Finnish Environment Institute SYKE, Natural Environment
Centre, Ecosystem Change Unit, P. O. Box 140, 00251 Helsinki, Finland;
4
Swiss Federal Institute for Forest, Snow and Landscape
Research, Community Ecology/Animal Ecology, Zuerchstrasse 111, 8903 Birmensdorf, Switzerland;
5
School of Human Science and
Environment, University of Hyogo, 1-1-12 Shinzaike-Honcho, Himeji City, Hyogo 670-0092, Japan;
6
Section of Biodiversity,
Department of Biology, University of Turku, 20014 Turku, Finland
ABSTRACT
Wood ants (Formica rufa group) are regarded as key-
stone species in boreal and mountain forests of Eur-
ope and Asia by their effect on ecosystem carbon (C)
and nutrient pools and fluxes. To quantify the impact
of their activity on boreal forest ecosystems, C,
nitrogen (N), phosphorus (P), potassium (K) and
calcium (Ca) pools and fluxes in wood ant nests
(WAN), and soil were assessed along a 5-, 30-, 60-,
and 100-year-old Norway spruce (Picea abies L. Kar-
sten) dominated successional gradient in eastern
Finland. Amounts of C and nutrients in WAN in-
creased with stand age,but contained less than 1% of
total C and nutrient pools in these stands. The CO
2
-
efflux from nests was also insignificant, as compared
to CO
2
-efflux from the forest floor. Annually, the
amount of C brought by wood ants into their nests as
honeydew, prey and nest-building materials ranged
from 2.7 to 49.3 kg ha
-1
C, but this is only 0.1–0.7%
of the combined net primary production of trees and
understorey in boreal forests. The difference between
wood ant nest C inputs and outputs was very small
in the younger-aged stands, and increased in the
older stands. Carbon accumulation rates in nests
over a 100 year period are estimated to be less than
10 kg ha
-1
a
-1
. In contrast to C, annual inputs of N,
P, and K are larger compared to wood ant nest
nutrient pool size, ranging from 3 to 6% of the
annual tree stand and understorey uptake. This
indicates a more rapid turnover and transport of N,
P, and K out of WAN, and suggests that wood ants
increase the cycling rate of these nutrients in boreal
forests.
Key words: ant nest; carbon balance; honeydew;
element cycling; Picea abies; prey; succession;
turnover.
INTRODUCTION
Wood ants (Formica rufa group) are keystone spe-
cies in boreal and mountain forests of Europe and
Received 20 June 2012; accepted 10 September 2012;
published online 27 October 2012
Author Contributions: All authors were involved in the design of the
study. Leena Fine
´r performed the calculations and wrote the paper with
significant input during the writing process from all other authors.
*Corresponding author; e-mail: leena.finer@metla.fi
Ecosystems (2013) 16: 196–208
DOI: 10.1007/s10021-012-9608-1
2012 Springer Science+Business Media New York
196

Asia (Ho
¨lldobler 1960; Rosengren and others 1979;
Laine and Niemela
¨1980), as they are considered to
be ecosystem engineers that affect carbon (C) and
nutrient pool sizes and fluxes (for example, Jones
and others 1994; Risch and others 2005). They
transfer C and nutrients from the forest floor to
their nests and from the nests back to the forest
floor and from the tree canopy to nests (Figure 1).
The area of forest floor and the number of trees
affected by ants as well as the magnitude of the
element transfer depend on the nest density
(number and size of nest ha
-1
), colony size
(number and size of workers), the extent of the
foraging area and the length of the growing season
available for the foraging within the forest ecosys-
tem (for example, Savolainen and Vepsa
¨la
¨inen
1988; Sorvari 2009). Wood ants collect plant litter,
preferably conifer needles, twigs and resin from the
forest floor to build large, long-lived nests on the
soil surface (for example, Wisniewski 1967; Lenoir
and others 1999). The diet of wood ants consists of
elements collected from different trophic levels:
honeydew excreted by aphids (Hemiptera, Aphi-
dina) living in the tree canopy, and invertebrate
prey from both the canopy and forest floor
(Ho
¨lldobler and Wilson 1990; Rosengren and
Sundstro
¨m1991; Domisch and others 2009). As
compared to prey, honeydew is low in nutrients
and mostly used as an energy source. In contrast,
prey is mainly needed for brood production (Des-
lippe and Savolainen 1994).
Although many studies have estimated C and
nutrient budgets in boreal forests including tree,
understory and soil components (for example,
Ma
¨lko
¨nen 1974; Helmisaari 1995; Fine
´r1989,
1991; Fine
´r and others 2003), none have included
ant nests or their C and nutrient fluxes. A few
studies have assessed C and nutrient pools in wood
ant nests (WAN) (Pokarzhevskij 1981; Risch and
others 2005; Kilpela
¨inen and others 2007), or C
and nutrient fluxes related to wood ant activity
(Zoebelein 1954; Horstmann 1974; Wellenstein
1980; Frouz and others 1997; Domisch and others
2009). These studies clearly indicate that C and
nutrient pools in WAN are a very small component
of total amounts in the forest floor or mineral soil
in boreal forests. However, WAN are localized C
and nutrient ‘‘hot spots’’, whose importance to
nutrient cycling may depend on the successional
stage of the forest stand (Ohashi and others 2012).
Earlier studies show that the amounts of phos-
phorus (P) and nitrogen (N) transferred to WAN as
honeydew and prey at the ecosystem level are 10–
60% of soil inputs from aboveground litterfall
(Frouz and others 1997; Domisch and others 2009).
This indicates that nutrients transferred to WAN
may be a significant ecosystem nutrient flux,
especially in young stands where annual tree lit-
terfall is small. Although the C and nutrient bal-
ances of WAN must be positive to allow the nest to
grow in size as the colony ages, we could not find
studies in which both pools and fluxes of WAN (as
shown in Figure 1) were used to estimate C and
nutrient accumulation rates in different-aged
stands. Such information is important to under-
stand the role of WAN imports and exports on C
and nutrient fluxes and cycling during stand suc-
cession after clear-cut harvesting, which is the
major disturbance agent in boreal forests of Europe
at present.
Therefore, the objectives of this paper are to:
(1) estimate the C, N, P, potassium (K) and calcium
(Ca) pool sizes, fluxes and accumulation rates in
WAN during forest succession and wood ant colony
development in different-aged Norway spruce
(Picea abies L. Karsten) stands, and (2) assess C and
nutrient fluxes of WAN in relation to fluxes from
other stand components during the growth and
development of a Norway spruce forest ecosystem.
This was accomplished by accessing comprehen-
sive, 3-year datasets of C and nutrient pools
and fluxes of WAN, and soil in Norway spruce-
dominated stands in eastern Finland.
MATERIALS AND METHODS
Study Sites
Most of the information used was obtained from a
series of published studies carried out in 16 Norway
Figure 1. A schematic presentation of the carbon and
nutrient pools and fluxes related to wood ant nests in
forest ecosystems. Evidence for and estimates of different
pools and fluxes are given in the results.
Wood Ants and Forest Ecosystem C and Nutrient Cycle 197

spruce-dominated forests of different successional
stages in eastern Finland (2952¢N, 6304¢E). The
tree stand, ant nest characteristics, and study
methods are described in detail by Kilpela
¨inen and
others (2008,2009), soil and ant nest properties by
Kilpela
¨inen and others (2007), Ohashi and others
(2007a) and Domisch and others (2008), CO
2
-
effluxes by Domisch and others (2006) and Ohashi
and others (2007b,2012), and ant dietary spectrum
and the selection of host trees by Domisch and
others (2009,2011). The age classes of the stands
were 5, 30, 60, and 100 years, with each age class
having four replicates. The numbers of active WAN
varied among age classes, ranging from 2.5 to
5.4 ha
-1
. Tree stem volume and volume growth in
different-aged stands ranged from 0 to 324 m
3
ha
-1
and 0–13.7 m
3
ha
-1
a
-1
, respectively (Kilpela
¨inen
and others 2008; Kilpela
¨inen and others 2009).
More detailed stand information is given in Table 1.
Carbon and Nutrient Pools and Fluxes
Vegetation
Pool sizes and fluxes of C and nutrients in living
trees, understory, WAN, and soil were estimated
separately for all of the stands.
Tree stem volumes measured in autumn 2003
and 2006 in the Norway spruce stands (Kilpela
¨inen
and others 2008) were used to calculate C and
nutrient pools in the aboveground components of
living trees with the equations from Palviainen and
Fine
´r(2011) for boreal forests. Stumps and coarse
root biomass and C pools were estimated in a
similar manner using the equations of Lehtonen
and others (2004), assuming a woody biomass C
content of 50%. Because no equations were
available for stumps and roots of deciduous trees,
the equations for Scots pine were used. The nutri-
ent pools of trees, stumps, and coarse roots were
estimated by multiplying biomass weights with the
nutrient concentrations presented by Fine
´r(1989).
Fine root C and nutrient pools were obtained from
the study of Ohashi and others (2007a) in the
Norway spruce stands. Carbon and nutrient con-
tent of fine root turnover were estimated to be
0.74% of the standing fine root biomass (Fine
´r and
others 2011). The annual accumulation of C and
nutrients in tree biomass was calculated as follows:
Ai= Pooli2006 Pooli2003=3ð1Þ
where A
i
is the annual accumulation of C, N, P, K
or Ca (kg ha
-1
a
-1
), and Pool
i
is C, N, P, K, or Ca
pool (kg ha
-1
) in tree biomass in 2006 or in 2003,
respectively, and 3, the number of growing sea-
sons.
The C pool of the understory was estimated with
the biomass equations presented by Muukkonen
and Ma
¨kipa
¨a
¨(2006) for boreal forests, and
assuming a 50% biomass C content. Understory
nutrient pools were obtained using nutrient con-
centrations of Kubin (1983) for boreal Norway
spruce-dominated forests. The C and nutrient
content of understory litterfall was estimated to be
25% of the standing biomass, as presented by
Ma
¨lko
¨nen (1974) for boreal forests.
Tree litterfall totals were estimated using the
equations of Saarsalmi and others (2007, Table 4,
Eq. 1). The amount of litterfall on the top of the
WAN was assumed to be proportional to nest basal
area, and assumed to have a C content of 50%.
Nutrient content of litterfall was calculated using
concentrations presented by Ukonmaanaho and
others (2008).
WAN and Soil
Pool sizes of C and nutrients in WAN and soil were
published by Kilpela
¨inen and others (2007) and
Ohashi and others (2007b). The input of C, N, P, K,
and Ca as honeydew, prey, and to the WAN in each
of the 30-, 60- and 100-year-old forest age stands
was obtained from a study by Domisch and others
(2009), which was based on measurements from
one medium-sized nest for 3 years (2003, 2004,
Table 1. Mean (±SD) Stand Characteristics in the Four Stand Age Classes (N=4)
Age
(years)
Area
(ha)
Number of
active
nests (ha
-1
)
Basal area
of active
nests (m
2
ha
-1
)
Stem volume Volume growth
(m
3
ha
-1
a
-1
)
Spr.
(%)
Pine
(%)
Dec.
(%)
Total
(m
3
ha
-1
)
5 5.8 (2.0) 2.5 (2.1) 2.0 (0.9) 0 0
30 5.1 (2.0) 3.2 (1.8) 2.6 (1.3) 79 6 15 163 (34) 16.3 (4.9)
60 6.5 (3.0) 5.4 (3.2) 6.6 (6.5) 84 10 6 229 (73) 12.4 (2.3)
100 7.9 (2.5) 4.1 (1.4) 8.7 (4.5) 73 20 7 324 (49) 9.8 (7.0)
Spr. = Norway spruce = Picea abies, Pine = Pinus sylvestris L., Dec. = deciduous trees, mainly Betula pendula Roth
198 L. Fine
´r and others

and 2005). Similar measurements were taken in
2003 and 2005 for one medium-sized wood ant
nest (0.13 m
3
) in one of the 5-year-old stands and
in all of the stands in 2003, 2004, and 2005 for all
nest-building materials (unpublished data).
The CO
2
-efflux from WAN was obtained from
the study of Ohashi and others (2012) in the four
stand age classes of the Norway spruce stands.
Carbon and nutrient inputs and C outputs as CO
2
from nests were extrapolated to stand level by
multiplying the results obtained per nest with the
nest density (number of WAN ha
-1
) for each stand.
Carbon and nutrient pools in soil and WAN were
obtained from Kilpela
¨inen and others (2007), and
soil C output (including fine roots) as CO
2
was
taken from Ohashi and others (2012) who did the
measurements in all of the Norway spruce stands.
RESULTS AND DISCUSSION
Changes in WAN Carbon Pools
and Fluxes with Stand Age
Carbon pools
WAN contained between 36 and 233 kg ha
-1
C, and
pool size was correlated with the age of the Norway
spruce-dominated stands (Table 2). Although WAN
age could not be determined in these stands, it was
assumed they were the same as the stand age. The
only other studies on wood ant nest C pools were by
Pokarzhevskij (1981), who reported a dry weight of
350 kg ha
-1
(corresponds to app. 175 kg ha
-1
of C)
of Formica polyctena WAN in a 50–60-year-old
temperate oak forest of the Russian Kursk region,
and by Risch and others (2005), who found
130–990 kg ha
-1
of C in WAN of Swiss subalpine
conifer forests varying in age from 165- to 236-years-
old. The size of the C pools seems to correlate posi-
tively with the volume of wood ant nest (Figure 2),
which increases with stand age (Rosengren and
others 1979; Vepsa
¨la
¨inen and Savolainen 1994;
Sorvari and Hakkarainen 2005; Kilpela
¨inen and
others 2005; Sorvari 2009). Wood ant nest age and
nest C accumulation rates can increase by stand age
(Table 3). The processes which control C accumu-
lation in nests with increasing stand age were in-
creased C input by wood ants and litterfall (Table 3),
and the decrease in nest decomposition rate (Dom-
isch and others 2008). An increase in wood ant nest
C accumulation rate with increasing stand age also
agrees with observations that ant population size
correlates with nest size, which increases with stand
succession (Sorvari and Hakkarainen 2005).
As shown in Table 2, WAN are small C pools
(<0.1%) even in the youngest forest age classes,
where soil and understorey were the main C pools.
Small wood ant nest C pools were also found in
Swiss subalpine forests (Risch and others 2005),
contributing only between 0.6 and 5% to total soil
C pools. Even though C pools in WAN were insig-
nificant at the ecosystem level, their C content was
6–10 times higher on an area basis (g m
-2
) than
the forest floor in the Finnish Norway spruce
stands, and 3–12 times higher in Swiss subalpine
forests (Risch and others 2005).
Carbon Inputs
Carbon is carried by wood ants into the nests as
honeydew, prey, resin, and plant litter. Additional
C is added to nests from aboveground litterfall and
fine root growth (Domisch and others 2009; Fig-
ure 3). Honeydew was the most important C input,
whereas plant material brought into the nests by
wood ants and litterfall accounted for 12 to 44% of
the annual nest C input. No other study reported
the C content of litter inputs to WAN, but the
amounts of litter components transported by wood
ants in these Norway spruce stands agree with mass
proportions reported for a wood ant colony in a
Finnish Scots pine forest (Rosengren and Sun-
dstro
¨m1991). Gibb and Johansson (2010) found
that wood ants harvest 18.8, 11.7, and 24.4 kg ha
-1
dry mass of honeydew during July in clear-cut
(1–4-years-old), middle-aged (30–40 years) and old
(80–100 years) Swedish boreal forests. Assuming
that half of the annual honeydew input occurs
in July, and is two-thirds of the total C input
(Figure 3) and using a C concentration for dry
honeydew of 43% (Domisch and others 2009), the
annual C inputs to WAN in northern Sweden are
24, 15, and 31 kg ha
-1
in clear-cut, middle-aged,
and old stands, respectively. The C honeydew
estimates for the middle-aged and old stands are
within the 95% confidence intervals of our Norway
spruce stands, but honeydew inputs in the Swedish
clear-cut stands are higher than the estimate for
our seedling stands. The WAN present in the
Swedish forests might have survived a few years
after clear-cut harvest, and consequently, honey-
dew transport remained at a relatively high level.
However, food resources were reduced in our
young Norway spruce seedling stand, and honey-
dew harvesting was decreased (Punttila and others
1991; Punttila 1996; Domisch and others 2005;
Sorvari and Hakkarainen 2007). The amounts of
honeydew carried into WAN are higher in tem-
perate forests, where a total of 13–216 kg ha
-1
a
-1
(dry mass) has been reported from a relatively
small number of stands (Horstmann 1974;
Wood Ants and Forest Ecosystem C and Nutrient Cycle 199

Wellenstein 1980; Frouz and others 1997 and ref-
erences therein).
Total C inputs into WAN from honeydew and
prey seem to increase with the age of the stand
(Figure 3), as does the tree stand productivity from
the 5-year-old stands compared to the older ones
(Tables 1,3). Because the availability of phloem
sap for aphids is related to the productivity of the
forest (Stadler and Michalzik 1998; Stadler and
others 1998), site quality can also affect the
amounts of honeydew C carried by wood ants into
their nests. It has been shown that the availability
of food plays an important role in determining the
abundance and sexual productivity of ant colonies
(Deslippe and Savolainen 1994). The C transported
to WAN is a reallocation of C within the ecosystem,
and is an insignificant (0.1–0.7%) amount of the C
fixed annually in net primary production (trees and
understorey combined) in boreal forests. This
explains why the harvesting of honeydew C from
Norway spruce canopies was not found to reduce
tree growth at the ecosystem level (Kilpela
¨inen and
others 2009).
Carbon Outputs
As shown in Table 3,CO
2
-efflux from WAN in
Finnish Norway spruce forests increased with stand
age (Table 3). Such a stand age effect was not
observed in older Swiss subalpine forests (Risch and
others 2005), where the age varied from 165 to
236 years. Most of the CO
2
-efflux likely comes from
wood ant respiration, and a lesser amount from
microbial decomposition of nest organic matter and
Table 2. Mean (±SD) Carbon, Nitrogen, Phosphorus, Potassium and Calcium Pools (kg ha
-1
) in Wood Ant
Nests (Including Above- and Belowground Components of Living Trees, and Understorey) and Soil Organic
Layer in the Norway Spruce Stands of Four Age Classes (N=4)
5 Years 30 Years 60 Years 100 Years
Carbon
Nests 36 (20) 40 (19) 135 (146) 233 (143)
Vegetation 2083 72901 93789 126449
Soil 32745 (5703) 25074 (3438) 29579 (4594) 27526 (2397)
Nitrogen
Nests 1.06 (0.56) 1.40 (0.54) 4.12 (4.60) 6.25 (3.56)
Vegetation 39.4 437.3 511.6 650.8
Soil 2203 (434) 2109 (243) 2313 (813) 1814 (157)
Phosphorus
Nests 0.036 (0.022) 0.045 (0.018) 0.154 (0.173) 0.255 (0.187)
Vegetation 20.0 67.5 90.7 101.9
Soil 52.7 (18.2) 45.7 (5.8) 43.3 (13.6) 38.4 (6.1)
Potassium
Nests 0.076 (0.056) 0.100 (0.038) 0.274 (0.236) 0.630 (0.455)
Vegetation 37.3 216.3 260.7 321.5
Soil 122 (68) 117 (40) 83.4 (22.8) 71.9 (10.2)
Calcium
Nests 0.247 (0.135) 0.821 (0.343) 1.520 (1.645) 2.284 (1.555)
Vegetation 73.8 476.0 558.7 674.4
Soil 364 (169) 358 (158) 272 (114) 267 (92)
Wood ant nest and soil data were taken from Kilpela
¨inen and others (2007)
Figure 2. Carbon (C) contents of wood ant nests in dif-
ferent forests in relation to nest volume (1) Kilpela
¨inen
and others (2007), (2) Pokarzhevskij (1981), (3) Risch
and others (2005).
200 L. Fine
´r and others

fine root respiration (Risch and others 2005; Domi-
sch and others 2006; Ohashi and others 2007b).
However, WAN in temperate forests may have
higher moisture contents than WAN in boreal forests
(Frouz and others 1997; Domisch and others 2008),
and organic matter mineralization in these nests
could contribute more to total nest CO
2
-efflux.
In contrast, no stand age-dependent trend was
found in the CO
2
-efflux from the forest floor in the
Finnish boreal or Swiss subalpine forests where,
however, all the study stands were much older
(165–236 years). The proportion of wood ant nest
CO
2
-efflux in total forest soil CO
2
-efflux increased
with stand age in Norway spruce forests, but the
contribution was marginal in both ecosystems:
0.03–0.5% in Norway spruce stands (Ohashi and
others 2012) and 0.7–2.7% in the subalpine forests
(Risch and others 2005) and the proportions would
have been even smaller if the CO
2
-effluxes from
soil coarse woody debris would have been mea-
sured in the studies and included in the forest soil
CO
2
-effluxes (Palviainen and others 2010).
Carbon Budget
The balance between C inputs and outputs as CO
2
was near zero in the two youngest stand age clas-
ses, and somewhat positive in the two oldest age
classes (Table 3); however, these C balance esti-
mates do not include C outputs in nongaseous
forms. To increase size and maintain nest vitality,
the long-term C balance of nests is positive,
otherwise nests would gradually collapse. These
estimated annual nest C accumulation rates are
close to the combined inputs of litter by wood ants
and litterfall on the nest surface (1–11 kg C ha
-1
a
-1
in boreal forests), both of which decompose
slowly (Lenoir and others 2001,2003; Domisch and
others 2008). In contrast, C inputs from honeydew
and prey are rapidly consumed, and quickly lost as
CO
2
by wood ant respiration. Similar C accumula-
tion rates (1–7 kg C ha
-1
a
-1
) were also calculated
by dividing the nest C pools by the age of the
stands. The comparable figures obtained with these
different methods indicate that the long-term C
Table 3. Mean (±SD) Annual Carbon Fluxes (kg ha
-1
a
-1
) in Wood Ant Nests, Aboveground Parts of Trees,
Understorey, Roots and Soil Organic Layer in the Norway Spruce Stands of Four Age Classes (N=4)
Flux 5 Years 30 Years 60 Years 100 Years
Nests
Input 2.7 (2.0) 12.4 (7.1) 36.7 (22.3) 49.3 (16.5)
Output 3.3 (1.6) 9.6 (5.6) 17.6 (10.4) 17.9 (5.9)
Trees
Accumulation 0 7011 (1998) 4968 (981) 3697 (1733)
Litterfall 0 591 (50) 692 (157) 678 (78)
Roots
Litterfall 227 252 283 322
Understorey
Litterfall 870 1287 1635 1948
Soil
Output 8360 (3035) 10738 (502) 9670 (1449) 11096 (1134)
Soil carbon fluxes were taken from Ohashi and others (2012)
Figure 3. Annual input
of carbon (C) in the wood
ant nests as honeydew,
prey, litter (mainly
needles and resin) and
litterfall (needle and fine
roots) in the different
stand age classes. Inputs
of honeydew and prey to
the nests are taken from
Domisch and others
(2009).
Wood Ants and Forest Ecosystem C and Nutrient Cycle 201

accumulation rates of WAN in boreal forests are
less than 10 kg ha
-1
a
-1
.
Changes in Wood Ant Nest Nutrient
Pools and Fluxes with Stand Age
Nutrient Pools
Similar to C, wood ant nest pools of N, P, K, and Ca
in Finnish Norway spruce increased with stand age
(Table 2). Except for Ca, the nutrient pools
increased with nest volume (Figure 4). Nutrients in
nests were a very small component of total nutrient
pools (<1%) in the boreal forests. However, on a
local area basis (g m
-2
), the nutrient content of
WAN in Finland and Switzerland were 3–11 times
higher than in the forest floor (Risch and others
2005, Kilpela
¨inen and others 2007).
Transport and Accumulation of Nutrients
The annual input of nutrients to WAN in boreal
Norway spruce forests followed the same stand age
related pattern as C (Table 4). More than 90% of N,
P and K were brought into nests as honeydew and
prey, which have higher nutrient concentrations
than plant litter used in nest construction (Domisch
and others 2009, Figure 5). Honeydew supplied
most of the N, P, and K to nests (59–84%), whereas
Ca contributions were similar for honeydew and
prey. However, Ca concentrations were higher in
Figure 4. Nitrogen (N), phosphorus (P), potassium (K) and calcium (Ca) contents of wood ant nests in different forests in
relation to nest volume (1) Kilpela
¨inen and others (2007), (2) Pokarzhevskij (1981), (3) Risch and others (2005).
202 L. Fine
´r and others

wood ant nest litter than honeydew and prey, and
supplied 27–73% of nest Ca. Frouz and others
(1997) reported that the annual input of P into
WAN was 1.725 kg ha
-1
in a temperate Czech
Republic Norway spruce plantation, and 78% was
transported as prey instead of honeydew. This was
higher than in Finnish boreal forests, and is likely
due to higher wood ant nest density in the Czech
plantation (0.2% of the soil surface area), com-
pared to 0.02–0.09% in the Finnish stands. In a
German oak forest, N input to WAN as honeydew
was 0.7 kg ha
-2
a
-1
(Horstmann 1974), which is
comparable to the two younger boreal Norway
spruce age classes. We could not find any other
studies in the literature which measured WAN
nutrient inputs.
Table 4. Mean (±SD) Annual Nitrogen, Phosphorus, Potassium and Calcium Fluxes (kg ha
-1
a
-1
)inWood
Ant Nests, Living Trees, Understorey, Roots and Soil Organic Layer in Norway Spruce Stands of Four Age
Classes (N=4)
5 Years 30 Years 60 Years 100 Years
Nitrogen
Nests
Input 0.20 (0.16) 1.11 (0.64) 4.87 (2.88) 4.86 (1.60)
Trees
Accumulation 0 38.4 (10.7) 25.2 (6.5) 17.4 (8.2)
Litterfall 0 14.9 (1.26) 17.7 (4.0) 16.7 (1.9)
Understorey
Litterfall 4.7 5.25 5.9 6.7
Roots
Litterfall 15.2 22.5 28.5 34.0
Phosphorus
Nests
Input 0.020 (0.016) 0.100 (0.057) 0.488 (0.288) 0.320 (0.105)
Trees
Accumulation 0 3.91 (1.04) 2.51 (0.64 1.68 (0.81)
Litterfall 0 1.75 (0.15) 2.08 (0.47 1.97 (0.23)
Understorey
Litterfall 0.55 0.61 0.68 0.77
Roots
Litterfall 1.31 1.94 2.47 2.94
Potassium
Nests
Input 0.039 (0.031) 0.169 (0.139) 0.755 (0.448) 0.522 (0.172)
Trees
Accumulation 0 16.6 (4.4) 10.8 (2.4 7.33 (3.6)
Litterfall 0 6.94 (0.59) 8.21 (1.87) 7.80 (0.89)
Understorey
Litterfall 1.32 1.46 1.64 1.87
Roots
Litterfall 2.37 3.51 4.45 5.30
Calcium
Nests
Input 0.007 (0.007) 0.078 (0.045) 0.148 (0.088) 0.149 (0.050)
Trees
Accumulation 0 37.6 (10.0) 23.7 (5.3) 15.6 (7.8)
Litterfall 0 6.1 (0.5) 7.2 (1.6) 6.8 (0.8)
Understorey
Litterfall 1.14 1.26 1.42 1.61
Roots
Litterfall 5.13 7.58 9.63 11.48
Figure 5. Annual transport of nitrogen (N), phosphorus
(P), potassium (K) and calcium (Ca) by wood ants into
nests as honeydew, prey, litter (mainly needles and re-
sin), and from litterfall on the nest surface in the different
stand age classes. (Fine roots were not included, because
the root nutrient uptake was assumed to take place inside
the nests). Inputs of honeydew and prey to the nests are
taken from Domisch and others (2009).
c
Wood Ants and Forest Ecosystem C and Nutrient Cycle 203

204 L. Fine
´r and others

The annual transport of N, P, and K into WAN was
large compared to the amounts of nutrients already
in the nests (Tables 2,4). This indicates that nutri-
ents are rapidly cycled, and there is a continuous
flow of nutrients out of the nests. We do not have
any information on the magnitude of these nutrient
flows, but there are a number of pathways by which
nutrients are removed from WAN: (1) ants remove
waste material (for example, dead bodies of ants,
prey remains, seeds, and so on) to garbage dumps
outside the nest (Mabelis 1979; Gorb and others
2000; Czechowski 2008 and references therein), (2)
ant-propagule production (sexual production, that
is, gynes and males) varies from year-to-year and
may constitute a large proportion of all reproductive
investments of a colony as was in a monogynous
population of Formica exsecta where an average of
73% of the spring brood and 85% of its biomass
were sexuals which leave the natal nest for dispersal
(Vitikainen and others 2011), in contrast to the
monogynous colonies, in polygynous colonies the
produced gynes mostly stay in their natal, often
multiple-nest colony, (3) predation on ants both on
the nest, especially in early spring by brown bear
and woodpeckers (Rolstad and others 1998; Swen-
son and others 1999) and on the foraging territory
by ants (Mabelis 1979) and other predators, (4)
other soil fauna in the WAN (Laakso and Seta
¨la
¨
1998; Lenoir and others 2003) move nutrients to the
surrounding soil and dispersing myrmecophiles to
other ant colonies (for example, Pa
¨ivinen and others
2002), (5) roots growing inside WAN (Ohashi and
others 2007a) translocate nutrients from WAN to
the aboveground, and (6) the fungi translocate
nutrients from decomposing nest organic matter
into the surrounding soil (Berg 1988; Boddy and
Watkinson 1995). The leaching of nutrients out of
WAN is probably insignificant, and does not
exceed nutrient input from atmospheric deposition,
because only the uppermost nest layers are affected by
rainfall and the rest of the nest remains dry (Frouz
1996; Lenoir and others 2001; Domisch and others
2008). The mineralization of N and P from litter used
for nest building is slow (Domisch and others 2008),
indicating that the N and P cycling rates are accel-
erated by wood ant activity. This might be especially
important in boreal forests, where N is often a
growth-limiting nutrient (for example, Tamm
1991). Eventually WAN are abandoned, the mois-
ture content of nest organic matter increases, and
they become hot spots for nutrient mineralization
(Lenoir and others 2001; Domisch and others 2008).
The annual transport of N, P, and K to WAN was
3–6% of the combined total annual flux in trees
and understory for the two oldest Norway spruce
age classes, whereas the proportions were smaller
(1%) in the two youngest age classes (Table 4).
The corresponding proportions for Ca fluxes were
even smaller, varying between 0.2 and 0.6% in the
different stand age classes. Frouz and others (1997)
calculated that more than 30% of the annual P flux
from the aboveground tree components to soil in a
temperate Norway spruce plantation is mediated
through WAN. If we make a similar calculation for
the Finnish boreal Norway spruce forests, 22–23%
of N and 14–19% of P fluxes from trees were
annually transported through WAN.
WAN as Carbon and Nutrient Hot Spots
The impact of wood ants in forest ecosystems is
spatially heterogeneous, and dependent on the
extent of their foraging area and nest density.
Based on a literature review by Risch and others
(2005), the number of WAN in most European
forests is less than 5 ha
-1
and seldom is greater
than 15 ha
-1
. The recent national forest invento-
ries in Finland show that the average wood ant nest
density of active nests is 3.19 ha
-1
(Punttila and
Kilpela
¨inen 2009). During forest succession wood
ant nest density varies less than nest size (Punttila
1996; Kilpela
¨inen and others 2008), which
increases with stand age (Domisch and others 2005;
Kilpela
¨inen and others 2008). Changes in wood ant
species composition during forest succession also
affect ant population size (Punttila 1996; Kilpela
¨i-
nen and others 2008).
The number and distribution pattern of WAN
increased the spatial variability of C and nutrients
in boreal Norway spruce forests, because their C
and nutrient content (g m
-2
) was 6–10 times
higher than in the forest floor. The foraging dis-
tance of wood ants from their nests depends on the
ant species and the size of the colonies. Early suc-
cessional stands have a higher diversity of wood
ants and other nest-building ant species, and the
nests (and colony population sizes) of these species
are usually much smaller than in later successional
stands (Kilpela
¨inen and others 2008; Sorvari 2009).
The foraging distance of smaller wood ant popula-
tions in younger stands extends only 10 m from
their nests, whereas in late successional stands with
larger colonies of species such as Formica aquilonia,
the dominant wood ant in Finnish Norway spruce
stands, foraging distances are much greater (Kil-
pela
¨inen and others 2008; Sorvari 2009; Table 5).
Using the equation presented by Sorvari (2009):
Y¼22:006 xþ14:985 ð2Þ
Wood Ants and Forest Ecosystem C and Nutrient Cycle 205

where Yis the distance to the most distant tree used
for foraging (m), and xis basal area of the nest
(m
2
), the average foraging distances in the 5-, 30-,
60- and 100-year-old Norway spruce stands are 33,
33, 41 and 61 m. Therefore, wood ants foraged in
85% of the total stand area in the youngest age
classes, and 100% of the stand in the older age
classes. However, in reality, the distribution of
wood ant activity in their foraging area is highly
uneven (for example, Figure 2in Savolainen and
Vepsa
¨la
¨inen 1989 and Figure 1in Niemela
¨and
others 1992), and nest densities are at their highest
near forest edges (Kilpela
¨inen and others 2008).
In Finnish boreal Norway spruce forests only a
very small proportion of trees (0.01–2.3%) is
visited by wood ants (Kilpela
¨inen and others
2009; Domisch and others 2011). As expected,
the percentage is higher near WAN, where up to
60% of the trees are visited within 20 m of the
nest (Vepsa
¨la
¨inen and Savolainen 1994; Domisch
and others 2011). This indicates that the C and
nutrient inputs to WAN come from very few
trees, the growth of which is significantly affected
by ants harvesting honeydew (Kilpela
¨inen and
others 2009). The indirect effects of wood ants on
canopy throughfall, soil nutrient mineralization,
hunting of invertebrates for prey, and C and
nutrient fluxes in and out of nests can also
impact the growth of other trees in the stand not
used by wood ants to tend aphids for honeydew
(for example, Stadler and others 2004; Jurgensen
and others 2008).
CONCLUSIONS
Wood ants had little impact on C pool size and efflux
in different-aged Norway spruce stands in Finland.
Carbon accumulation rates in WAN over a 100-year
period are estimated to be less than 10 kg ha
-1
a
-1
.
The annual transport of N, P, and K into nests was
large compared to nest pool size and 3–6% of the
annual stand uptake, which indicates that these
nutrients are rapidly cycled, and there is a continu-
ous flow of nutrients out of nests. Thus, WAN are
localized ‘‘hot spots’’ for nutrient cycling, and can
affect the spatial distribution of C and nutrient fluxes
within boreal forest ecosystems.
ACKNOWLEDGMENTS
This study was funded by the Academy of Finland
(Projects: 200870 and 114380).
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