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.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Wood ants (Formica rufa group) are keystone species in boreal and mountain forests of Europe and Asia (Hölldobler 1960; Rosengren and others 1979; Laine and Niemelä 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 ecosystem (for example, Savolainen and Vepsäläinen 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, Aphidina) living in the tree canopy, and invertebrate prey from both the canopy and forest floor (Hölldobler and Wilson 1990; Rosengren and Sundström 1991; 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 (Deslippe and Savolainen 1994).
Although many studies have estimated C and nutrient budgets in boreal forests including tree, understory and soil components (for example, Mälkönen 1974; Helmisaari 1995; Finér 1989, 1991; Finér 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; Kilpeläinen 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 phosphorus (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 litterfall is small. Although the C and nutrient balances 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 understand the role of WAN imports and exports on C and nutrient fluxes and cycling during stand succession 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 comprehensive, 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 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 Kilpeläinen and others (2008, 2009), soil and ant nest properties by Kilpeläinen and others (2007), Ohashi and others (2007a) and Domisch and others (2008), CO2-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 m3 ha−1 and 0–13.7 m3 ha−1 a−1, respectively (Kilpeläinen and others 2008; Kilpeläinen 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 (Kilpeläinen and others 2008) were used to calculate C and nutrient pools in the aboveground components of living trees with the equations from Palviainen and Finér (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 nutrient pools of trees, stumps, and coarse roots were estimated by multiplying biomass weights with the nutrient concentrations presented by Finér (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 content of fine root turnover were estimated to be 0.74% of the standing fine root biomass (Finér and others 2011). The annual accumulation of C and nutrients in tree biomass was calculated as follows:
where A i is the annual accumulation of C, N, P, K or Ca (kg ha−1 a−1), and Pooli 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 seasons.
The C pool of the understory was estimated with the biomass equations presented by Muukkonen and Mäkipää (2006) for boreal forests, and assuming a 50% biomass C content. Understory nutrient pools were obtained using nutrient concentrations 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 Mälkönen (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 Kilpeläinen 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, and 2005). Similar measurements were taken in 2003 and 2005 for one medium-sized wood ant nest (0.13 m3) 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 CO2-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 CO2 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 Kilpeläinen and others (2007), and soil C output (including fine roots) as CO2 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 positively with the volume of wood ant nest (Figure 2), which increases with stand age (Rosengren and others 1979; Vepsäläinen and Savolainen 1994; Sorvari and Hakkarainen 2005; Kilpeläinen 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 accumulation in nests with increasing stand age were increased C input by wood ants and litterfall (Table 3), and the decrease in nest decomposition rate (Domisch 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 insignificant 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; Figure 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 Sundström 1991). 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, honeydew transport remained at a relatively high level. However, food resources were reduced in our young Norway spruce seedling stand, and honeydew 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 temperate 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; Wellenstein 1980; Frouz and others 1997 and references 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 (Kilpeläinen and others 2009).
Carbon Outputs
As shown in Table 3, CO2-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 CO2-efflux likely comes from wood ant respiration, and a lesser amount from microbial decomposition of nest organic matter and fine root respiration (Risch and others 2005; Domisch 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 CO2-efflux.
In contrast, no stand age-dependent trend was found in the CO2-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 CO2-efflux in total forest soil CO2-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 CO2-effluxes from soil coarse woody debris would have been measured in the studies and included in the forest soil CO2-effluxes (Palviainen and others 2010).
Carbon Budget
The balance between C inputs and outputs as CO2 was near zero in the two youngest stand age classes, and somewhat positive in the two oldest age classes (Table 3); however, these C balance estimates 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 CO2 by wood ant respiration. Similar C accumulation 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 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, Kilpeläinen 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 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), compared 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.
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 nutrients 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; Swenson and others 1999) and on the foraging territory by ants (Mabelis 1979) and other predators, (4) other soil fauna in the WAN (Laakso and Setälä 1998; Lenoir and others 2003) move nutrients to the surrounding soil and dispersing myrmecophiles to other ant colonies (for example, Päivinen 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 accelerated 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 moisture 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 inventories in Finland show that the average wood ant nest density of active nests is 3.19 ha−1 (Punttila and Kilpeläinen 2009). During forest succession wood ant nest density varies less than nest size (Punttila 1996; Kilpeläinen and others 2008), which increases with stand age (Domisch and others 2005; Kilpeläinen and others 2008). Changes in wood ant species composition during forest succession also affect ant population size (Punttila 1996; Kilpeläinen 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 distance of wood ants from their nests depends on the ant species and the size of the colonies. Early successional 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 (Kilpeläinen and others 2008; Sorvari 2009). The foraging distance of smaller wood ant populations 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 (Kilpeläinen and others 2008; Sorvari 2009; Table 5). Using the equation presented by Sorvari (2009):
where Y is the distance to the most distant tree used for foraging (m), and x is basal area of the nest (m2), 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 2 in Savolainen and Vepsäläinen 1989 and Figure 1 in Niemelä and others 1992), and nest densities are at their highest near forest edges (Kilpeläinen 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 (Kilpeläinen 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 (Vepsäläinen 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 (Kilpeläinen 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 continuous 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.
References
Adlung KG. 1966. A critical evaluation of the European research on use of red wood ants (Formica rufa group) for the protection of forests against harmful insects. J Appl Entomol 57:167–89.
Berg B. 1988. Dynamics of nitrogen (15N) in decomposing Scots pine (Pinus sylvestris) needle litter. Can J Bot 66:1539–46.
Boddy L, Watkinson SC. 1995. Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73(Suppl 1):S1377–83.
Czechowski W. 2008. Around-nest “cemeteries” of Myrmica schencki Em. (Hymenoptera : Formicidae): their origin and a possible significance. Pol J Ecol 56:359–63.
Deslippe RJ, Savolainen R. 1994. Role of food supply in structuring a population of Formica ants. J Anim Ecol 63:756–64.
Domisch T, Finér L, Jurgensen MF. 2005. Red wood ant nest densities in managed boreal forests. Ann Zool Fennici 42:277–82.
Domisch T, Finér L, Ohashi M, Risch AC, Sundström L, Niemelä P, Jurgensen MF. 2006. Contribution of red wood ant mounds to forest floor CO2 efflux in boreal coniferous forests. Soil Biol Biochem 38:2425–33.
Domisch T, Ohashi M, Finér L, Risch AC, Sundström L, Kilpeläinen J, Niemelä P. 2008. Decomposition of organic matter and nutrient mineralisation in wood ant (Formica rufa group) nests in boreal coniferous forests of different age. Biol Fertil Soils 44(3):539–45.
Domisch T, Finér L, Neuvonen S, Niemelä P, Risch AC, Kilpeläinen J, Ohashi M, Jurgensen MF. 2009. Foraging activity and dietary spectrum of wood ants (Formica rufa group) and their role in nutrient fluxes in boreal forests. Ecol Entomol 34:369–77.
Domisch T, Neuvonen S, Sundström L, Punttila P, Finér L, Kilpeläinen J, Niemelä P, Risch AC, Ohashi M, Jurgensen MF. 2011. Sources of variation in the incidence of ant-aphid mutualism in boreal forests. Agric For Entomol 13:239–45.
Finér L. 1989. Biomass and nutrient cycle in fertilized and unfertilized pine, mixed birch and pine and spruce stand on a fertilized mire. Acta For Fennica 208:1–63.
Finér L. 1991. Effect of fertilization on dry mass accumulation and nutrient cycling in Scots pine on an ombrotrophic bog. Acta For Fennica 223:1–42.
Finér L, Mannerkoski H, Piirainen S, Starr M. 2003. Carbon and nitrogen pools in an old-growth, Norway spruce mixed forest in eastern Finland and changes associated with clear-cutting. For Ecol Manag 174:51–63.
Finér L, Ohashi M, Noguchi K, Hirano Y. 2011. Fine root production and turnover in forest ecosystems in relation to stand and environmental characteristics. For Ecol Manag 262:2008–23.
Frouz J. 1996. The role of nest moisture in thermoregulation of ant (Formica polyctena, Hymenoptera, Formicidae) nests. Biologia 51(5):541–7.
Frouz J, Šantrůčková H, Kalčík J. 1997. The effect of wood ants (Formica polyctena Foerst.) on the transformation of phosphorus in a spruce plantation. Pedobiologia 41:437–47.
Gibb H, Johansson T. 2010. Forest succession and harvesting of hemipteran honeydew by boreal ants. Ann Zool Fennici 47:99–110.
Gorb SN, Gorb EV, Punttila P. 2000. Effects of redispersal of seeds by ants on the pattern in a deciduous forest: a case study. Acta Oecol 21:293–301.
Helmisaari H-S. 1995. Nutrient cycling in Pinus sylvestris stands in eastern Finland. Plant Soil 168–169:327–36.
Hölldobler B. 1960. Über die Ameisenfauna in Finnland-Lappland. Waldhygiene 3:229–38.
Hölldobler B, Wilson EO. 1990. The ants. Berlin: Springer. 732 p
Horstmann K. 1974. Untersuchungen über den Nahrungserwerb der Waldameisen (Formica polyctena Foerster) im Eichenwald III. Jahresbilanz. Oecologia 15:187–204.
Jones CG, Lawton JH, Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69:373–86.
Jurgensen MF, Finér L, Domisch T, Kilpeläinen J, Punttila P, Ohashi M, Niemelä P, Sundström L, Neuvonen S, Risch AC. 2008. Organic nest-building ants: their impact on soil properties in temperate and boreal forests. J Appl Entomol 132:266–75.
Kilpeläinen J, Punttila P, Sundström L, Niemelä P, Finér L. 2005. Forest stand structure, site type and distribution of ant nests in boreal forests in Finland in the 1950s. Ann Zool Fennici 42(3):243–58.
Kilpeläinen J, Finér L, Niemelä P, Domisch T, Neuvonen S, Ohashi M, Risch AC, Sundström L. 2007. Carbon, nitrogen and phosphorus dynamics of ant nests (Formica rufa group) in managed boreal forests of different successional stages. Appl Soil Ecol 36:156–63.
Kilpeläinen J, Punttila P, Finér L, Niemelä P, Domisch T, Jurgensen MF, Neuvonen S, Ohashi M, Risch AC, Sundström L. 2008. Distribution of ant species and nests (Formica) in different-aged managed spruce stands in eastern Finland. J Appl Entomol 132:315–25.
Kilpeläinen J, Finér L, Neuvonen S, Niemelä P, Domisch T, Risch AC, Jurgensen MF, Ohashi M, Sundström L. 2009. Does the mutualism between wood ants (Formica rufa group) and Cinara aphids affect Norway spruce growth? For Ecol Manag 257:238–43.
Kubin E. 1983. Nutrients in the soil, ground and tree layer in an old spruce forest in Northern Finland. Ann Bot Fennici 20:361–90.
Laakso J, Setälä H. 1998. Composition and trophic structure of detrital food web in ant nest mounds of Formica aquilonia and in the surrounding forest soil. Oikos 81:266–78.
Laine KJ, Niemelä P. 1980. The influence of ants on the survival of mountain birches during Oporinia autumnata (Lep., Geometridae) outbreak. Oecologia 47:39–42.
Lehtonen A, Mäkipää R, Heikkinen J, Sievänen R, Liski J. 2004. Biomass expansion factors (BEFs) for Scots pine, Norway spruce and birch according to stand age for boreal forests. For Ecol Manag 188:211–24.
Lenoir L, Bengtsson J, Persson T. 1999. Effects of coniferous resin on fungal biomass and mineralization processes in wood ant nest materials. Biol Fertil Soils 30:251–7.
Lenoir L, Persson T, Bengtsson J. 2001. Wood ant nests as potential hot spots for carbon and nitrogen mineralisation. Biol Fertil Soils 34:235–40.
Lenoir L, Bengtsson J, Persson T. 2003. Effects of conifer resin on soil fauna in potential wood-ant nest materials at different moisture levels. Pedobiologia 47:19–25.
Mabelis AA. 1979. Wood ant wars—the relationship between aggression and predation in the red wood ant (Formica polyctena Först.). Neth J Zool 29:451–620.
Mälkönen E. 1974. Annual primary production and nutrient cycle in some Scots pine stands. Commun Inst For Fenniae 84(5):1–87.
Muukkonen P, Mäkipää R. 2006. Empirical biomass models of understorey in boreal forests according to stand age and site attributes. Boreal Environ Res 11:355–69.
Niemelä J, Haila Y, Halme E, Pajunen T, Punttila P. 1992. Small-scale heterogeneity in the spatial distribution of carabid beetles in the southern Finnish taiga. J Biogeogr 19:173–81.
Ohashi M, Kilpeläinen J, Finér L, Risch AC, Domisch T, Neuvonen S, Niemelä P. 2007a. The effect of red wood ant (Formica rufa group) mounds on root biomass, density, and nutrient concentrations in boreal managed forests. J For Res 12:113–19.
Ohashi M, Finér L, Domisch T, Risch AC, Jurgensen MF, Niemelä P. 2007b. Seasonal and diurnal CO2 efflux from red wood ant (Formica aquilonia) nests in boreal coniferous forests. Soil Biol Biochem 39:1504–11.
Ohashi M, Domisch T, Finér L, Jurgensen MF, Sundström L, Kilpeläinen J, Risch AC, Niemelä P. 2012. The effect of stand age on CO2 efflux from wood ant (Formica rufa group) mounds in boreal forests. Soil Biol Biochem 52:21–8.
Päivinen J, Ahlroth P, Kaitala V. 2002. Ant-associated beetles of Fennoscandia and Denmark. Entomol Fennica 13:20–40.
Palviainen M, Finér L, Laiho R, Shorohova E, Kapitsa E, Vanha-Majamaa I. 2010. Carbon and nitrogen release from decomposing Scots pine, Norway spruce and silver birch stumps. For Ecol Manag 259:390–8.
Palviainen M, Finér L. 2011. Estimation of nutrient removals in stem-only and whole-tree harvesting of Scots pine, Norway spruce, and birch stands with generalized nutrient equations. Eur J For Res 131:945–64.
Pokarzhevskij AD. 1981. The distribution and accumulation of nutrients in nests of ant Formica polyctena (Hymenoptera, Formicidae). Pedobiologia 21:117–24.
Punttila P. 1996. Succession, forest fragmentation, and the distribution of wood ants. Oikos 75:291–8.
Punttila P, Haila Y, Pajunen T, Tukia H. 1991. Colonization of clear-cut forests by ants in the southern Finnish taiga: a quantitative survey. Oikos 61:250–62.
Punttila P, Kilpeläinen J. 2009. Distribution of nest-building ant species (Formica spp., Hymenopter) in Finland: preliminary results of a national survey. Ann Zool Fennici 46:1–15.
Risch AC, Jurgensen MF, Schütz M, Page-Dumroese DS. 2005. The contribution of red wood ants to soil C and N pools and CO2 emissions in subalbine forests. Ecology 86(2):419–30.
Rolstad J, Majewski P, Rolstad E. 1998. Black woodpecker use of habitats and feeding substrates in a managed Scandinavian forest. J Wildl Manag 62:11–23.
Rosengren R, Vepsäläinen K, Wuorenrinne H. 1979. Distribution, nest densities, and ecological significance of wood ants (the Formica rufa group) in Finland. Bulletin Section Regionale Ouest Paleartique/West Palaearctic Regional Section Bulletin, Organisation Internationale de Lutte Biologique Controle les Animaux et les Plantes Nuisible/International Organization for the Biological Control of Noxious Animals and Plants II-3:181–213.
Rosengren R, Sundström L. 1991. The interaction between red wood ants, Cinara aphids and pines. A ghost of mutualism past? In: Huxley CR, Cutler DF, Eds. Ant–plant interaction. Oxford: Oxford University Press. p 80–91.
Saarsalmi A, Starr M, Hokkanen T, Ukonmaanaho L, Kukkola M, Nöjd P, Sievänen R. 2007. Predicting annual canopy litterfall production for Norway spruce (Picea abies (L.) Karst.) stands. For Ecol Manag 242:578–86.
Savolainen R, Vepsäläinen K. 1988. A competition hierarchy among boreal ants—impact on resource partitioning and community structure. Oikos 51:135–55.
Savolainen R, Vepsäläinen K. 1989. Niche differentiation of ant species within territories of the wood ant Formica polyctena. Oikos 56:3–16.
Sorvari J. 2009. Foraging distances and potentiality in forest pest insect control: an example with two candidate ants (Hymenoptera: Formicidae). Myrmecol News 12:211–15.
Sorvari J, Hakkarainen H. 2005. Deforestation reduces nest mound size and decreases the production of sexual offspring in the wood ant Formica aquilonia. Ann Zool Fennici 42:259–67.
Sorvari J, Hakkarainen H. 2007. Wood ants are wood ants: deforestation causes population declines in the polydomous wood ant Formica aquilonia. Ecol Entomol 32:707–11.
Stadler B, Michalzik B. 1998. Aphid infested Norway spruce are “hot spots” in throuhgfall carbon chemistry in coniferous forests. Can J For Res 28:1717–22.
Stadler B, Michalzik B, Müller T. 1998. Linking aphid ecology with nutrient fluxes in a coniferous forest. Ecology 79(5):1514–25.
Stadler B, Mühlenberger E, Michalzik B. 2004. The ecology driving nutrient fluxes in forests. In: Weisser WW, Siwmann E, Eds. Insects and Ecosystem function. Springer, Berlin. Ecol Stud 173:213–39.
Swenson JE, Jansson A, Riig R, Sandegren F. 1999. Bears and ants: myrmecophagy by brown bears in central Scandinavia. Can J Zool 77:551–61.
Tamm CO. 1991. Nitrogen in terrestrial ecosystems: questions of productivity, al changes, and ecosystem stability. Springer, Berlin. Ecol Stud 81:11.
Ukonmaanaho L, Merilä P, Nöjd P, Nieminen TM. 2008. Litterfall production and nutrient return to the forest floor in Scots pine and Norway spruce stands in Finland. Boreal Environ Res 13(Suppl B):67–91.
Vepsäläinen K, Savolainen R. 1994. Ant-aphid interaction and territorial dynamics of wood ants. Memorab Zool 48:251–9.
Vitikainen E, Haag-Liautard C, Sundström L. 2011. Inbreeding and reproductive investment in the ant Formica exsecta. Evolution 65:2026–37.
Wellenstein G. 1980. Auswirkung hügelbauender waldameisen der Formica rufa-gruppe auf forstschädliche raupen und das wachstum der waldbäume. Zeitschrift für Angewandte Entomologie 89:114–57.
Wisniewski J. 1967. Die Zusammensetzung des Baumaterials der Nesthügel von Formica polyctena in Kiefernwäldern. Waldhygienie 7:117–21.
Zoebelein G. 1954. Versuche zur Feststellung des Honigtauertrages von Fichtenbeständen mit Hilfe von Waldameisen. Zeitschrift für Angewandte Entomologie 36:358–62.
Acknowledgments
This study was funded by the Academy of Finland (Projects: 200870 and 114380).
Author information
Authors and Affiliations
Corresponding author
Additional information
Author Contributions
All authors were involved in the design of the study. Leena Finér performed the calculations and wrote the paper with significant input during the writing process from all other authors.
Rights and permissions
About this article
Cite this article
Finér, L., Jurgensen, M.F., Domisch, T. et al. The Role of Wood Ants (Formica rufa group) in Carbon and Nutrient Dynamics of a Boreal Norway Spruce Forest Ecosystem. Ecosystems 16, 196–208 (2013). https://doi.org/10.1007/s10021-012-9608-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-012-9608-1