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Carbon, nitrogen and phosphorus dynamics of ant mounds (Formica rufa group) in managed boreal forests of different successional stages
applied soil ecology 36 (2007) 156–163
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Carbon, nitrogen and phosphorus dynamics of ant mounds (Formica rufa group) in managed boreal forests of different successional stages J. Kilpela¨inen a,*, L. Fine´r a, P. Niemela¨ b, T. Domisch a, S. Neuvonen a, M. Ohashi a, A.C. Risch c, L. Sundstro¨m d a
Finnish Forest Research Institute, Joensuu Research Unit, P.O. Box 68, FI-80101 Joensuu, Finland University of Joensuu, Faculty of Forestry, P.O. Box 111, FI-80101 Joensuu, Finland c Swiss Federal Institute for Forest, Snow and Landscape Research, Community Ecology, Zuercherstrasse 111, 8903 Birmensdorf, Switzerland d University of Helsinki, Department of Biological and Environmental Sciences, Ecology and Evolutionary Biology Unit, P.O. Box 65, FI-00014 Helsinki, Finland b
article info
abstract
Article history:
Wood ants (Formica rufa group) are ubiquitous in European boreal forests and their large
Received 29 September 2006
long-lived mound nests, which mainly consist of forest litter and resin, accumulate carbon
Received in revised form
(C) and nutrients. The C and nutrient dynamics of wood ant mounds in response to forest
22 January 2007
succession have received minor attention in boreal forests. We aimed to study whether the
Accepted 24 January 2007
C, nitrogen (N) and phosphorus (P) concentrations and the bulk density of ant mounds differ from those of the surrounding forest soil, to estimate the C, N and P pools in ant mounds, and to test whether the concentrations and pools change with forest age. Norway spruce
Keywords:
(Picea abies (L.) Karst.) stands on medium-fertile sites in 5-, 30-, 60- and 100-year stand age
Boreal forest
classes were studied in eastern Finland. Carbon and P concentrations in the above-ground
Formica rufa group
mound material were higher than those in the surrounding organic layer. The C, N and
Carbon
extractable P concentrations were higher in the soil under the ant mounds than in the
Nitrogen
surrounding mineral soil (0–21 cm). The low bulk densities in the ant mounds and the soil
Phosphorus
below them could be a result of the porous structure of ant mounds and the soil-mixing
Bulk density
activities of the ants. The C/N ratios were higher in the mounds than in the organic layer. Carbon concentrations in the ant mounds increased slightly with stand age. Carbon, N and P pools in the ant mounds increased considerably with stand age. Carbon, N and P pools in ant mounds were <1% of those in the surrounding forest soil. Nevertheless, the above- and belowground parts of the ant mounds contained more C, N and P per sampled area than the surrounding forest soil. Wood ants therefore increase the spatial heterogeneity in C and nutrient distribution at the ecosystem level. # 2007 Elsevier B.V. All rights reserved.
1.
Introduction
Wood ants (Formica rufa group) are a prominent feature in the boreal forests of Eurasia. Ants build their mounds from forest
litter and tree resin droplets, and they use honeydew and insects and small invertebrates as their food source. On average three mounds per hectare occur in the most common forest site types in Finland (Rosengren et al., 1979; Domisch
* Corresponding author. Tel.: +358 10 211 3177; fax: +358 10 211 3001. E-mail address: [email protected] (J. Kilpela¨inen). 0929-1393/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2007.01.005
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applied soil ecology 36 (2007) 156–163
et al., 2005; Kilpela¨inen et al., 2005). Most of the boreal forests in Fennoscandia are managed and forest succession starts from clear-cutting. This can be destructive for ant colonies because it removes food resources and changes the microclimatic conditions (Rosengren et al., 1979). Ants often abandon their mounds within a few years after clear-cutting, but new mounds are soon established and the composition of wood ant species may change during forest succession (e.g. Punttila, 1996). Ant mounds remain active in the same locations for several years, sometimes even for decades. The results of studies in temperate and alpine forests in Europe indicate that ants can play a significant role in nutrient cycling and aggregation (e.g. Frouz et al., 1997) but, so far, their contribution to element pools and fluxes have not been studied in boreal forests (see Laakso and Seta¨la¨, 1998). Studies on active ant mounds in temperate, hemi-boreal and subalpine areas (Zakharov et al., 1981; Lenoir et al., 2001; Frouz et al., 2005; Risch et al., 2005) report only carbon (C), nitrogen (N), phosphorus (P) concentrations and/or bulk densities of the above-ground mound material, and they do not investigate the effects of forest succession on element concentrations or pools. The C and nutrient concentrations in ant mounds can be higher than those in the surrounding soil (Zakharov et al., 1981; Lenoir et al., 2001; Risch et al., 2005) due to the extensive flow of prey (Stradling, 1978), honeydew (Rosengren and Sundstro¨m, 1991) and mound constructing material (Rosengren and Sundstro¨m, 1987) into the mound, and the high number of nitrogen-fixing bacteria (Frouz et al., 1997) and other soil microbes (Laakso and Seta¨la¨, 1998) living in the mounds. Obviously the type of material used for construction also affects the chemical properties of ant mounds. Nutrient concentrations in the organic layer of forest soils decrease during forest succession (Tamminen, 1991) and, if the nutrient concentrations of the mound material are primarily dependent on the surrounding litter, the nutrient concentrations in ant mounds could thus also decrease during succession. The total C and nutrient pools in ant mounds; however, are likely to increase during forest succession because ant mound and ant densities are higher in older stands (Sorvari and Hakkarainen, 2005), and
the ants have had more time to build larger mounds. There are no estimates of the contribution of ant mounds to the total element pools in boreal forest soil (cf. Risch et al., 2005). Bulk density could indicate ant colony vitality since in recently clear-cut sites severely depleted colonies may not be able to keep their mounds in good condition and aerated, which could result in on average higher bulk densities of mounds in clear-cut sites than in mature sites. Dense and less active mounds can decompose faster than dry and porous active mounds (Lenoir et al., 2001). Thus forest management, ant colony vitality, bulk density, decomposition and C and nutrient concentrations and pools of ant mounds could be related. The aim of the study was to determine whether the C, N and P concentrations and the bulk density of active ant mounds differ from those of the surrounding forest soil, and whether such differences relate to forest age. We also assessed and compared the C, N and P pools in active ant mounds in forests of different age.
2.
Material and methods
2.1.
Study sites
The study was carried out in four replicate 5-, 30-, 60- and 100year-old stands (2.3–11.3 ha) growing on medium-fertile (Myrtillus type according to the Finnish site type classification by Cajander, 1949) sites in eastern Finland (298520 E, 638040 N, 170 m a.s.l.). The 16 stands were managed as Norway spruce (Picea abies (L.) Karst.) stands. Although only Norway spruce was planted in the 5-, 30-, and 60-year-old stands, deciduous trees and Scots pine (Pinus sylvestris L.) are numerous in the early successional stages (Table 1). The 100-year-old stands were naturally regenerated because at that time planting was rare. The stands were managed according to normal practices including thinning at appropriate times. The soil type in the sites was haplic podzol (FAO-Unesco, 1990) on glacial till and the organic layer was on the average 8 cm thick. The stands contained an average of 3.8 active ant mounds ha1 (Table 2).
Table 1 – Mean tree number (haS1), height (cm) and stem volume (m3 haS1) and their standard errors (in parentheses) in the different stand age classes (n = 4) Age (years)
Picea abies
Pinus sylvestris
Betula spp.
Populas tremula
Alnus incana – –
Sorbus aucuparia
Total
5
Trees Height
1727 (104) 52 (3)
1610 (1129) 37 (4)
13397 (3363) 65 (7)
192 (120) 66 (25)
8547 (4415) 82 (3)
25,473 (7490) –
30
Trees Volume
1258 (228) 128 (10)
95 (87) 11 (10)
149 (49) 19 (10)
8 (5) 0 (0)
249 (55) 4 (2)
25 (25) 0 (0)
1,784 (289) 163 (17)
60
Trees Volume
760 (147) 192 (51)
128 (103) 23 (16)
134 (75) 7 (5)
69 (66) 7 (6)
52 (49) 0 (0)
– –
1,143 (363) 229 (36)
100
Trees Volume
708 (232) 237 (34)
103 (65) 65 (39)
97 (39) 21 (13)
9 (7) 0 (0)
31 (24) 1 (1)
– –
949 (193) 325 (24)
The measured trees in seedling stands were 20 cm tall, and in the other stands 4 cm thick at breast height. Height describes the stand structure in the 5-year stand age class.
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applied soil ecology 36 (2007) 156–163
Table 2 – Mean numbers and volumes of active ant mounds in the individual stand age classes Age (years) 5 30 60 100
Number (ha1) 2.5 3.2 5.4 4.1
(1.0) (0.9) (1.6) (0.7)
Volume (dm3) 147 237 417 1062
(37) (36) (41) (86)
Standard errors are in parentheses.
2.2.
Sampling
All the ant mounds in the 16 stands were inventoried and their heights and diameters measured during summer 2003. After the inventory, we sorted the active ant mounds within stand age classes by volume and selected sample mounds randomly from certain fractiles: 60, 70, 80 and 90% in the 5-year; 45, 60, 75 and 90% in the 30- and 60-year; 30, 50, 70 and 90% in the 100year age class. The volume range of the sample mounds was 63–2353 dm3. One to three ant mounds were sampled in each stand. Most of the ant mounds were inhabited by F. aquilonia Yarr., but F. polyctena Fo¨rst. inhabited one of the ant mounds in the 30-year stand age class and F. rufa L. one mound each in the 5- and 30-year age classes. The ant mounds had a moist surface layer, a dryer and looser interior, and a transition from mixed organic/mineral to mineral soil belowground. Three core samples were taken from the aboveground parts of each ant mound with a stainless steel corer with a diameter of 14 cm: one sample was taken at the centre of the mound, one at the edge of the mound and one in between the centre and edge (Fig. 1). The depths of the core samples were measured from the exposed ant mound, the lowest point of the sample being the level of the uppermost mineral soil around the ant mound. One belowground soil sample was taken under each of the three aboveground ant mound samples to a depth of 21 cm with a cylindrical sampler with a diameter of 72 mm and length 49 mm. Four samples were taken from the forest soil at points 3 m from the ant mound edge in north, west, south and east directions (Fig. 1). We assumed that ant mounds did not
Fig. 1 – Sampling design: (1) above-ground mound, (2) surrounding organic layer, (3) soil under mound and (4) surrounding mineral soil. The organic layer and mineral soil were sampled in four positions around each ant mound.
have any significant effect on the nutrient concentrations in forest soil at this distance (Karhu and Neuvonen, 1998). The organic layer was sampled with a stainless steel borer with a diameter of 14 cm, and the depth of the layer was measured to an accuracy of 0.5 cm. A mineral soil sample (E horizon and the upper part of B horizon) was taken below the sampled organic layer in the same way as the soil sampling under the ant mounds. The four forest soil samples were combined by layer for the nutrient analyses.
2.3.
Analyses and calculations
Stones, cones, dead branches, etc. with a diameter >2 cm were separated from the samples and their mass and volume subtracted from the corresponding values for the samples. The samples were dried to constant weight at 40 8C. The samples taken below the ant mounds and from the mineral soil were sieved through a 2-mm sieve, and both fractions were weighed. Nutrients were determined on the <2 mm fraction. The samples from the ant mounds and organic layer were milled before analysis. The total C and N concentrations in all the samples dried at 40 8C were determined with a LECO CHN-1000 analyzer. The samples from the ant mounds and organic layer were wet-digested in HNO3–H2O2 and their total P concentration (dry matter basis, i.e. dried at 105 8C) determined by ICP-AES (inductively coupled plasma-atomic emission spectrometry). The samples taken below the ant mounds and from the mineral soil were extracted with ammonium acetate (pH 4.65) and the extractable P concentration (dry matter basis) was determined by the molybdate-hydrazine method (Halonen et al., 1983) on a spectrophotometer (Perkin-Elmer Lambda 11). Ant mound volumes (dm3) were calculated using the equation of a half ellipsoid. The C and nutrient pools in the ant mounds were calculated by multiplying the average nutrient concentrations of the sampled ant mounds in each stand by the area-based ant mound masses.
2.4.
Statistical analyses
Linear mixed models (SPSS 14.0.1 for Windows) and Bonferroni multiple comparisons were used to test for significant differences in C and nutrient concentrations, C/N ratios and bulk density between the fixed factors, stand age classes and sample loci, and their interaction. Forest stand was used as a random factor. Among the sample loci, (1) ant mounds versus soil organic layer and (2) soil under ant mound versus mineral soil, were tested separately. The same analysis was performed for the C, N and P pools m2. To reduce heteroscedasticity, P concentrations and C/N ratios of the organic layer and ant mounds were ln(x + 1) transformed before analysis. The C and P concentrations of mineral soil and soil under ant mounds were ln(x + 1) transformed, and N concentrations of the same samples ln(ln(x + 1)) transformed. One-way ANOVA and Bonferroni multiple comparisons were applied to compare the C, N and P pools ha1 of ant mounds between stand age classes. Nutrient pools were ln(x + 1) transformed to retain normal distribution and equal variances between stand age classes.
applied soil ecology 36 (2007) 156–163
Mean nutrient pools of the above-ground parts of active ant mounds are presented per mound base areas and per hectare. The results were considered statistically significant when the significance level was a < 0.05.
3.
Results
3.1.
C, N and P concentrations, bulk density
Both the C and P concentrations were higher in the aboveground ant mound material than in the surrounding organic
159
layer (F1,28 = 128.1, p < 0.001 and F1,28 = 74.2, p < 0.001, respectively), but the total N concentrations did not differ significantly (Fig. 2). The C concentrations in above-ground ant mound and surrounding organic layer were higher in the 100year than in the 30-year stand age class (F3,13 = 4.7, p = 0.021). Similarly, the concentrations of C, N and extractable P in the soil below the ant mounds were significantly higher than those in the surrounding mineral soil (F1,28 = 86.4, p < 0.001; F1,28 = 81.6, p < 0.001; F1,28 = 111.2, p < 0.001, respectively) (Fig. 2). In the 30- and 60-year stand age classes, the bulk density of the ant mound material was lower than that in the
Fig. 2 – Mean C, N and P concentrations (dry matter basis) and bulk density and their standard errors in ant mounds and surrounding organic layer (left) in different stand age classes (n = 4), and the same for C, N and extractable P concentrations and bulk density in soil under ant mounds and surrounding mineral soil (right). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively. Note the different y-scales.
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applied soil ecology 36 (2007) 156–163
surrounding organic layer (F3,28 = 6.0, p = 0.003, Bonferroni’s p < 0.017) (Fig. 2). In the 60- and 100-year stand age classes, the soil under the ant mounds had a lower bulk density than the surrounding mineral soil (F3,28 = 3.1, p = 0.044, Bonferroni’s p < 0.004) (Fig. 2).
3.2.
C, N and P pools
The above-ground parts of the ant mounds contained more C (F1,28 = 175.1, p < 0.001), N (F1,28 = 109.5, p < 0.001) and P/m2 (F1,28 = 114.2, p < 0.001) than the surrounding organic layer (Fig. 3). In the 100-year stand age class the above-ground parts of the ant mounds had more C/m2 than in the 5- and 30-year age classes (F3,28 = 7.4, p = 0.001, Bonferroni’s p < 0.004). The soil under the ant mounds had more C (F1,28 = 223.5, p < 0.001) and N/m2 (F1,28 = 203.9, p < 0.001) than the surrounding mineral soil. On a hectare basis, the C (F3,12 = 5.9, p = 0.010, Bonferroni’s p = 0.016), N (F3,12 = 4.9, p = 0.019, Bonferroni’s p = 0.023) and P (F3,12 = 5.1, p = 0.017, Bonferroni’s p = 0.022) pools in the ant mounds were higher in the 100-year age class than those in the 5-year class, and the C pool in the 100-year age class was higher than that in the 30-year age class (Bonferroni’s p = 0.042) (Table 3). The C, N and P pools in the organic layer
and in the mineral soil were many times higher than the pools in the above-ground part of the ant mounds or the soil under the ant mounds (Table 3).
3.3.
C/N ratio
The C/N ratio was higher in the above-ground parts of the ant mounds than in the organic layer (F1,28 = 84.0, p < 0.001) (Fig. 4). The C/N ratio did not differ between the soil under the ant mounds and the surrounding mineral soil.
4.
Discussion
In this study, the C, N and P concentrations in the aboveground parts of the ant mounds were similar to those reported for ant mounds in a coniferous forest in the Moscow region, Russia (Zakharov et al., 1981). The C and N concentrations and the C/N ratios were almost similar to those in the ant mounds in subalpine coniferous forests in Switzerland (Risch et al., 2005). In the Swiss subalpine forests both the C and N concentrations were higher in the ant mounds than in the surrounding forest soil, but the C/N ratios showed no difference (Risch et al., 2005). As was the case in this study,
Fig. 3 – Mean C, N and P pools and their standard errors in ant mounds and surrounding organic layer (left), and C and N pools in soil under ant mound and surrounding mineral soil down to 21 cm depth (right) in different stand age classes (n = 4). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively.
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Table 3 – Mean C, N and P pools (kg haS1) in ant mounds, soil under ant mounds (0–21 cm), organic layer and mineral soil (0–21 cm) in the different stand age classes (n = 4) Age (years)
Sample locus
C
N
P
5
Above-ground mound Soil under mound Organic layer Mineral soil
25a 11 32,745 24,644
(8) (3) (5703) (2836)
0.5a (0.2) 0.5 (0.2) 1034 (183) 1170 (138)
0.04a (0.01) – 53 (9) –
30
Above-ground mound Soil under mound Organic layer Mineral soil
26a 14 25,074 23,499
(6) (3) (3438) (3452)
0.7 (0.1) 0.7 (0.2) 929 (153) 1179 (98)
0.05 (0.01) – 46 (3) –
60
Above-ground mound Soil under mound Organic layer Mineral soil
93 42 29,579 31,946
(49) (24) (4594) (7736)
2.1 (1.1) 2.0 (1.2) 933 (137) 1380 (337)
0.15 (0.09) – 43 (7) –
100
Above-ground mound Soil under mound Organic layer Mineral soil
180b 53 27,526 21,741
(63) (10) (2397) (5440)
3.7b (1.3) 2.6 (0.5) 817 (83) 997 (142)
0.25b (0.09) – 38 (3) –
Standard errors are in parentheses. Only the data indexed with different letters differ significantly ( p < 0.05) between stand age classes, only pools in ant mounds were tested.
the C/N ratio was higher in the ant mounds than in the organic layer in boreal coniferous and mixed forests in central Sweden (Lenoir et al., 2001), which implies that the material in the ant mounds was less decomposed than that in the surrounding organic layer. Low C/nutrient ratios usually indicate a fast decomposition rate (Berg and McClaugherty, 2003) but, for instance, N mineralization from decomposing litter can be associated with initially higher C/N ratios in mature forests than in clear-cut areas (Berg and Ekbohm, 1983). The ant mound material is selectively collected from the forest floor by ants, and in coniferous stands primarily consists of conifer needles. Norway spruce needle litter, which is common mound-building material, usually has lower N and P concentrations (Berg and Tamm, 1991; Johansson, 1995; Lundmark-Thelin and Johansson, 1997; Berg et al., 2000) than the ant mound material (Zakharov et al., 1981; Lenoir et al., 2001; Frouz et al., 2005; Risch et al., 2005), and therefore the presence of other ant mound material explains the higher nutrient concentrations. Ant mounds contain relatively more resin particles (Lenoir et al., 1999) and food remains than the surrounding organic layer. The soil microbe (Frouz et al., 1997; Laakso and Seta¨la¨, 1998) and root composition (Farji-Brener,
2000; Ohashi et al., in press) of ant mounds also differ from those in the surrounding soil, and they may have an impact on the C and nutrient concentrations. In a temperate forest in the Czech Republic, a higher N fixing bacterial assemblage was found in the ant mounds compared to the surrounding organic layer (Frouz et al., 1997). However, this was probably not the case in our study because the N concentrations were similar in the ant mounds and in the surrounding organic layer. Laakso and Seta¨la¨ (1998) found a larger soil animal biomass, suggesting a higher amount of resources, in ant mounds than in the surrounding forest soil in Finland, but no differences in the N and P concentrations between the surface layers of ant mounds and the surrounding litter layer. Fine root N and P concentrations were higher in ant mounds than in the surrounding organic layer (Ohashi et al., in press). Ants themselves have also been reported to affect litter quality (Stadler et al., 2006). Furthermore, the organic layer comprises the whole decomposition continuum from litter to humus, while the material in the ant mounds is less decomposed and younger. The higher C, N and extractable P concentrations in the soil under the ant mounds compared to the surrounding mineral soil might be explained by the input of organic material caused
Fig. 4 – Mean C/N ratios and their standard errors of ant mounds and surrounding organic layer, and soil under ant mounds and surrounding mineral soil in different stand age classes (n = 4). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively.
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by the mixing activity of the ants, whilst nutrient leaching by percolation water is highly unlikely in the dry conditions of ant mounds. Also in Denmark, higher C, N (Kristiansen and Amelung, 2001) and P (Kristiansen et al., 2001) concentrations were found under the abandoned ant mounds than in the surrounding soil. Our results did not support the hypothesis that the nutrient concentrations would decrease in ant mounds simultaneously with the decreases in the surrounding soil during forest succession. In our study, nutrient concentrations in the organic layer did not decrease during forest succession, which was the opposite of earlier findings in boreal forests in southern Finland (Tamminen, 1991). Actually the C concentrations in the ant mounds increased slightly along with increasing stand age. The bulk densities of the ant mounds in subalpine forests in Switzerland (Risch et al., 2005) were similar to our values. The bulk densities in the above- and below-ground parts of the ant mounds were lower than in the surrounding soil. The interior of the mounds of the Formica rufa group is known to have a porous structure with ant tunnels and chambers, and the mineral soil under the mounds is also mixed with organic matter by the ants, resulting in a lower bulk density. There were no significant stand-age related differences in the bulk densities of the ant mounds although the bulk density seemed to be highest in the seedling stands. This might indicate reduced ant activity in the recently clear-cut sites, which leads to accelerated decomposition. The contribution of ant mounds to the total C, N and P pools in the forest soil was small (<1%), and smaller than that in the subalpine forests in Switzerland where it was 0.6–5% of the C and N pools in organic layer depending on the forest type (Risch et al., 2005). The pools in ant mounds may seem negligible when extrapolated to the ecosystem level. However, ant mounds were shown to increase the spatial heterogeneity in the distribution of C, N and P in forest soil, and this might also affect e.g. nutrient availability to the trees. The results of this study also show that more nutrients are accumulated in ant mounds along with forest succession.
Acknowledgements We acknowledge the technical help of Ms. Laura Ikonen, Mr. Teuvo Vauhkala, Ms. Anita Pussinen, Ms. Seija Repo, Ms. Anki Geddala, Dr. Sirpa Piirainen and Ms. Maini Mononen. We thank Mr. Pekka Punttila for identification of the ant species and Mr. Jaakko Heinonen for statistical advice. Thanks go to Dr. John Derome for revising the text. We appreciate the comments of two anonymous reviewers. The Academy of Finland (project 200870) financed the study.
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Punttila, P., 1996. Succession, forest fragmentation, and the distribution of wood ants. Oikos 75, 291–298. Risch, A.C., Jurgensen, M.F., Schu¨tz, M., Page-Dumroese, D.S., 2005. The contribution of red wood ants to soil C and N pools and to CO2 emissions in subalpine forests. Ecology 86, 419–430. Rosengren, R., Sundstro¨m, L., 1987. The foraging system of a red wood ant colony (Formica s. str.)—collecting and defending food through an extended phenotype. In: Pasteels, J.M., Deneubourg, J.L. (Eds.), From Individual to Collective Behaviour on Social Insects. Experimentia 54 (Suppl.), 117–137. Rosengren, R., Sundstro¨m, L., 1991. The interaction between red wood ants, Cinara aphids and pines. A ghost of mutualism past? In: Huxley, C.R., Cutler, D.F. (Eds.), Ant–Plant Interactions. Oxford University Press, Oxford, New York, Tokyo, pp. 80–91. Rosengren, R., Vepsa¨la¨inen, K., Wuorenrinne, H., 1979. Distribution, nest densities, and ecological significance of wood ants (the Formica rufa group) in Finland. O.I.L.B. Bull. SROP II-3, 183–213.
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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. Fenn. 42, 259–267. Stadler, B., Schramm, A., Kalbitz, K., 2006. Ant-mediated effects on spruce litter decomposition, solution chemistry, and microbial activity. Soil Biol. Biochem. 38, 561–572. Stradling, D.J., 1978. Food and feeding habits of ants. In: Brian, M.V. (Ed.), Production Ecology of Ants and Termites. Cambridge University Press, Cambridge, pp. 81–106. Tamminen, P., 1991. Kangasmaan ravinnetunnusten ilmaiseminen ja viljavuuden alueellinen vaihtelu Etela¨Suomessa. Expression of soil nutrient status and regional variation in soil fertility of forested sites in southern Finland (in Finnish, with English abstract). Folia Forestalia 777 40 pp. Zakharov, A.A., Ivanickaja, E.F., Maksimova, A.E., 1981. Accumulation of nutrients in nests of Formica sp. (Hymenoptera, Formicidae) (in Russian, with English abstract). Pedobiologia 21, 36–45.
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/apsoil
Carbon, nitrogen and phosphorus dynamics of ant mounds (Formica rufa group) in managed boreal forests of different successional stages J. Kilpela¨inen a,*, L. Fine´r a, P. Niemela¨ b, T. Domisch a, S. Neuvonen a, M. Ohashi a, A.C. Risch c, L. Sundstro¨m d a
Finnish Forest Research Institute, Joensuu Research Unit, P.O. Box 68, FI-80101 Joensuu, Finland University of Joensuu, Faculty of Forestry, P.O. Box 111, FI-80101 Joensuu, Finland c Swiss Federal Institute for Forest, Snow and Landscape Research, Community Ecology, Zuercherstrasse 111, 8903 Birmensdorf, Switzerland d University of Helsinki, Department of Biological and Environmental Sciences, Ecology and Evolutionary Biology Unit, P.O. Box 65, FI-00014 Helsinki, Finland b
article info
abstract
Article history:
Wood ants (Formica rufa group) are ubiquitous in European boreal forests and their large
Received 29 September 2006
long-lived mound nests, which mainly consist of forest litter and resin, accumulate carbon
Received in revised form
(C) and nutrients. The C and nutrient dynamics of wood ant mounds in response to forest
22 January 2007
succession have received minor attention in boreal forests. We aimed to study whether the
Accepted 24 January 2007
C, nitrogen (N) and phosphorus (P) concentrations and the bulk density of ant mounds differ from those of the surrounding forest soil, to estimate the C, N and P pools in ant mounds, and to test whether the concentrations and pools change with forest age. Norway spruce
Keywords:
(Picea abies (L.) Karst.) stands on medium-fertile sites in 5-, 30-, 60- and 100-year stand age
Boreal forest
classes were studied in eastern Finland. Carbon and P concentrations in the above-ground
Formica rufa group
mound material were higher than those in the surrounding organic layer. The C, N and
Carbon
extractable P concentrations were higher in the soil under the ant mounds than in the
Nitrogen
surrounding mineral soil (0–21 cm). The low bulk densities in the ant mounds and the soil
Phosphorus
below them could be a result of the porous structure of ant mounds and the soil-mixing
Bulk density
activities of the ants. The C/N ratios were higher in the mounds than in the organic layer. Carbon concentrations in the ant mounds increased slightly with stand age. Carbon, N and P pools in the ant mounds increased considerably with stand age. Carbon, N and P pools in ant mounds were <1% of those in the surrounding forest soil. Nevertheless, the above- and belowground parts of the ant mounds contained more C, N and P per sampled area than the surrounding forest soil. Wood ants therefore increase the spatial heterogeneity in C and nutrient distribution at the ecosystem level. # 2007 Elsevier B.V. All rights reserved.
1.
Introduction
Wood ants (Formica rufa group) are a prominent feature in the boreal forests of Eurasia. Ants build their mounds from forest
litter and tree resin droplets, and they use honeydew and insects and small invertebrates as their food source. On average three mounds per hectare occur in the most common forest site types in Finland (Rosengren et al., 1979; Domisch
* Corresponding author. Tel.: +358 10 211 3177; fax: +358 10 211 3001. E-mail address: [email protected] (J. Kilpela¨inen). 0929-1393/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2007.01.005
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applied soil ecology 36 (2007) 156–163
et al., 2005; Kilpela¨inen et al., 2005). Most of the boreal forests in Fennoscandia are managed and forest succession starts from clear-cutting. This can be destructive for ant colonies because it removes food resources and changes the microclimatic conditions (Rosengren et al., 1979). Ants often abandon their mounds within a few years after clear-cutting, but new mounds are soon established and the composition of wood ant species may change during forest succession (e.g. Punttila, 1996). Ant mounds remain active in the same locations for several years, sometimes even for decades. The results of studies in temperate and alpine forests in Europe indicate that ants can play a significant role in nutrient cycling and aggregation (e.g. Frouz et al., 1997) but, so far, their contribution to element pools and fluxes have not been studied in boreal forests (see Laakso and Seta¨la¨, 1998). Studies on active ant mounds in temperate, hemi-boreal and subalpine areas (Zakharov et al., 1981; Lenoir et al., 2001; Frouz et al., 2005; Risch et al., 2005) report only carbon (C), nitrogen (N), phosphorus (P) concentrations and/or bulk densities of the above-ground mound material, and they do not investigate the effects of forest succession on element concentrations or pools. The C and nutrient concentrations in ant mounds can be higher than those in the surrounding soil (Zakharov et al., 1981; Lenoir et al., 2001; Risch et al., 2005) due to the extensive flow of prey (Stradling, 1978), honeydew (Rosengren and Sundstro¨m, 1991) and mound constructing material (Rosengren and Sundstro¨m, 1987) into the mound, and the high number of nitrogen-fixing bacteria (Frouz et al., 1997) and other soil microbes (Laakso and Seta¨la¨, 1998) living in the mounds. Obviously the type of material used for construction also affects the chemical properties of ant mounds. Nutrient concentrations in the organic layer of forest soils decrease during forest succession (Tamminen, 1991) and, if the nutrient concentrations of the mound material are primarily dependent on the surrounding litter, the nutrient concentrations in ant mounds could thus also decrease during succession. The total C and nutrient pools in ant mounds; however, are likely to increase during forest succession because ant mound and ant densities are higher in older stands (Sorvari and Hakkarainen, 2005), and
the ants have had more time to build larger mounds. There are no estimates of the contribution of ant mounds to the total element pools in boreal forest soil (cf. Risch et al., 2005). Bulk density could indicate ant colony vitality since in recently clear-cut sites severely depleted colonies may not be able to keep their mounds in good condition and aerated, which could result in on average higher bulk densities of mounds in clear-cut sites than in mature sites. Dense and less active mounds can decompose faster than dry and porous active mounds (Lenoir et al., 2001). Thus forest management, ant colony vitality, bulk density, decomposition and C and nutrient concentrations and pools of ant mounds could be related. The aim of the study was to determine whether the C, N and P concentrations and the bulk density of active ant mounds differ from those of the surrounding forest soil, and whether such differences relate to forest age. We also assessed and compared the C, N and P pools in active ant mounds in forests of different age.
2.
Material and methods
2.1.
Study sites
The study was carried out in four replicate 5-, 30-, 60- and 100year-old stands (2.3–11.3 ha) growing on medium-fertile (Myrtillus type according to the Finnish site type classification by Cajander, 1949) sites in eastern Finland (298520 E, 638040 N, 170 m a.s.l.). The 16 stands were managed as Norway spruce (Picea abies (L.) Karst.) stands. Although only Norway spruce was planted in the 5-, 30-, and 60-year-old stands, deciduous trees and Scots pine (Pinus sylvestris L.) are numerous in the early successional stages (Table 1). The 100-year-old stands were naturally regenerated because at that time planting was rare. The stands were managed according to normal practices including thinning at appropriate times. The soil type in the sites was haplic podzol (FAO-Unesco, 1990) on glacial till and the organic layer was on the average 8 cm thick. The stands contained an average of 3.8 active ant mounds ha1 (Table 2).
Table 1 – Mean tree number (haS1), height (cm) and stem volume (m3 haS1) and their standard errors (in parentheses) in the different stand age classes (n = 4) Age (years)
Picea abies
Pinus sylvestris
Betula spp.
Populas tremula
Alnus incana – –
Sorbus aucuparia
Total
5
Trees Height
1727 (104) 52 (3)
1610 (1129) 37 (4)
13397 (3363) 65 (7)
192 (120) 66 (25)
8547 (4415) 82 (3)
25,473 (7490) –
30
Trees Volume
1258 (228) 128 (10)
95 (87) 11 (10)
149 (49) 19 (10)
8 (5) 0 (0)
249 (55) 4 (2)
25 (25) 0 (0)
1,784 (289) 163 (17)
60
Trees Volume
760 (147) 192 (51)
128 (103) 23 (16)
134 (75) 7 (5)
69 (66) 7 (6)
52 (49) 0 (0)
– –
1,143 (363) 229 (36)
100
Trees Volume
708 (232) 237 (34)
103 (65) 65 (39)
97 (39) 21 (13)
9 (7) 0 (0)
31 (24) 1 (1)
– –
949 (193) 325 (24)
The measured trees in seedling stands were 20 cm tall, and in the other stands 4 cm thick at breast height. Height describes the stand structure in the 5-year stand age class.
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applied soil ecology 36 (2007) 156–163
Table 2 – Mean numbers and volumes of active ant mounds in the individual stand age classes Age (years) 5 30 60 100
Number (ha1) 2.5 3.2 5.4 4.1
(1.0) (0.9) (1.6) (0.7)
Volume (dm3) 147 237 417 1062
(37) (36) (41) (86)
Standard errors are in parentheses.
2.2.
Sampling
All the ant mounds in the 16 stands were inventoried and their heights and diameters measured during summer 2003. After the inventory, we sorted the active ant mounds within stand age classes by volume and selected sample mounds randomly from certain fractiles: 60, 70, 80 and 90% in the 5-year; 45, 60, 75 and 90% in the 30- and 60-year; 30, 50, 70 and 90% in the 100year age class. The volume range of the sample mounds was 63–2353 dm3. One to three ant mounds were sampled in each stand. Most of the ant mounds were inhabited by F. aquilonia Yarr., but F. polyctena Fo¨rst. inhabited one of the ant mounds in the 30-year stand age class and F. rufa L. one mound each in the 5- and 30-year age classes. The ant mounds had a moist surface layer, a dryer and looser interior, and a transition from mixed organic/mineral to mineral soil belowground. Three core samples were taken from the aboveground parts of each ant mound with a stainless steel corer with a diameter of 14 cm: one sample was taken at the centre of the mound, one at the edge of the mound and one in between the centre and edge (Fig. 1). The depths of the core samples were measured from the exposed ant mound, the lowest point of the sample being the level of the uppermost mineral soil around the ant mound. One belowground soil sample was taken under each of the three aboveground ant mound samples to a depth of 21 cm with a cylindrical sampler with a diameter of 72 mm and length 49 mm. Four samples were taken from the forest soil at points 3 m from the ant mound edge in north, west, south and east directions (Fig. 1). We assumed that ant mounds did not
Fig. 1 – Sampling design: (1) above-ground mound, (2) surrounding organic layer, (3) soil under mound and (4) surrounding mineral soil. The organic layer and mineral soil were sampled in four positions around each ant mound.
have any significant effect on the nutrient concentrations in forest soil at this distance (Karhu and Neuvonen, 1998). The organic layer was sampled with a stainless steel borer with a diameter of 14 cm, and the depth of the layer was measured to an accuracy of 0.5 cm. A mineral soil sample (E horizon and the upper part of B horizon) was taken below the sampled organic layer in the same way as the soil sampling under the ant mounds. The four forest soil samples were combined by layer for the nutrient analyses.
2.3.
Analyses and calculations
Stones, cones, dead branches, etc. with a diameter >2 cm were separated from the samples and their mass and volume subtracted from the corresponding values for the samples. The samples were dried to constant weight at 40 8C. The samples taken below the ant mounds and from the mineral soil were sieved through a 2-mm sieve, and both fractions were weighed. Nutrients were determined on the <2 mm fraction. The samples from the ant mounds and organic layer were milled before analysis. The total C and N concentrations in all the samples dried at 40 8C were determined with a LECO CHN-1000 analyzer. The samples from the ant mounds and organic layer were wet-digested in HNO3–H2O2 and their total P concentration (dry matter basis, i.e. dried at 105 8C) determined by ICP-AES (inductively coupled plasma-atomic emission spectrometry). The samples taken below the ant mounds and from the mineral soil were extracted with ammonium acetate (pH 4.65) and the extractable P concentration (dry matter basis) was determined by the molybdate-hydrazine method (Halonen et al., 1983) on a spectrophotometer (Perkin-Elmer Lambda 11). Ant mound volumes (dm3) were calculated using the equation of a half ellipsoid. The C and nutrient pools in the ant mounds were calculated by multiplying the average nutrient concentrations of the sampled ant mounds in each stand by the area-based ant mound masses.
2.4.
Statistical analyses
Linear mixed models (SPSS 14.0.1 for Windows) and Bonferroni multiple comparisons were used to test for significant differences in C and nutrient concentrations, C/N ratios and bulk density between the fixed factors, stand age classes and sample loci, and their interaction. Forest stand was used as a random factor. Among the sample loci, (1) ant mounds versus soil organic layer and (2) soil under ant mound versus mineral soil, were tested separately. The same analysis was performed for the C, N and P pools m2. To reduce heteroscedasticity, P concentrations and C/N ratios of the organic layer and ant mounds were ln(x + 1) transformed before analysis. The C and P concentrations of mineral soil and soil under ant mounds were ln(x + 1) transformed, and N concentrations of the same samples ln(ln(x + 1)) transformed. One-way ANOVA and Bonferroni multiple comparisons were applied to compare the C, N and P pools ha1 of ant mounds between stand age classes. Nutrient pools were ln(x + 1) transformed to retain normal distribution and equal variances between stand age classes.
applied soil ecology 36 (2007) 156–163
Mean nutrient pools of the above-ground parts of active ant mounds are presented per mound base areas and per hectare. The results were considered statistically significant when the significance level was a < 0.05.
3.
Results
3.1.
C, N and P concentrations, bulk density
Both the C and P concentrations were higher in the aboveground ant mound material than in the surrounding organic
159
layer (F1,28 = 128.1, p < 0.001 and F1,28 = 74.2, p < 0.001, respectively), but the total N concentrations did not differ significantly (Fig. 2). The C concentrations in above-ground ant mound and surrounding organic layer were higher in the 100year than in the 30-year stand age class (F3,13 = 4.7, p = 0.021). Similarly, the concentrations of C, N and extractable P in the soil below the ant mounds were significantly higher than those in the surrounding mineral soil (F1,28 = 86.4, p < 0.001; F1,28 = 81.6, p < 0.001; F1,28 = 111.2, p < 0.001, respectively) (Fig. 2). In the 30- and 60-year stand age classes, the bulk density of the ant mound material was lower than that in the
Fig. 2 – Mean C, N and P concentrations (dry matter basis) and bulk density and their standard errors in ant mounds and surrounding organic layer (left) in different stand age classes (n = 4), and the same for C, N and extractable P concentrations and bulk density in soil under ant mounds and surrounding mineral soil (right). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively. Note the different y-scales.
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applied soil ecology 36 (2007) 156–163
surrounding organic layer (F3,28 = 6.0, p = 0.003, Bonferroni’s p < 0.017) (Fig. 2). In the 60- and 100-year stand age classes, the soil under the ant mounds had a lower bulk density than the surrounding mineral soil (F3,28 = 3.1, p = 0.044, Bonferroni’s p < 0.004) (Fig. 2).
3.2.
C, N and P pools
The above-ground parts of the ant mounds contained more C (F1,28 = 175.1, p < 0.001), N (F1,28 = 109.5, p < 0.001) and P/m2 (F1,28 = 114.2, p < 0.001) than the surrounding organic layer (Fig. 3). In the 100-year stand age class the above-ground parts of the ant mounds had more C/m2 than in the 5- and 30-year age classes (F3,28 = 7.4, p = 0.001, Bonferroni’s p < 0.004). The soil under the ant mounds had more C (F1,28 = 223.5, p < 0.001) and N/m2 (F1,28 = 203.9, p < 0.001) than the surrounding mineral soil. On a hectare basis, the C (F3,12 = 5.9, p = 0.010, Bonferroni’s p = 0.016), N (F3,12 = 4.9, p = 0.019, Bonferroni’s p = 0.023) and P (F3,12 = 5.1, p = 0.017, Bonferroni’s p = 0.022) pools in the ant mounds were higher in the 100-year age class than those in the 5-year class, and the C pool in the 100-year age class was higher than that in the 30-year age class (Bonferroni’s p = 0.042) (Table 3). The C, N and P pools in the organic layer
and in the mineral soil were many times higher than the pools in the above-ground part of the ant mounds or the soil under the ant mounds (Table 3).
3.3.
C/N ratio
The C/N ratio was higher in the above-ground parts of the ant mounds than in the organic layer (F1,28 = 84.0, p < 0.001) (Fig. 4). The C/N ratio did not differ between the soil under the ant mounds and the surrounding mineral soil.
4.
Discussion
In this study, the C, N and P concentrations in the aboveground parts of the ant mounds were similar to those reported for ant mounds in a coniferous forest in the Moscow region, Russia (Zakharov et al., 1981). The C and N concentrations and the C/N ratios were almost similar to those in the ant mounds in subalpine coniferous forests in Switzerland (Risch et al., 2005). In the Swiss subalpine forests both the C and N concentrations were higher in the ant mounds than in the surrounding forest soil, but the C/N ratios showed no difference (Risch et al., 2005). As was the case in this study,
Fig. 3 – Mean C, N and P pools and their standard errors in ant mounds and surrounding organic layer (left), and C and N pools in soil under ant mound and surrounding mineral soil down to 21 cm depth (right) in different stand age classes (n = 4). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively.
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Table 3 – Mean C, N and P pools (kg haS1) in ant mounds, soil under ant mounds (0–21 cm), organic layer and mineral soil (0–21 cm) in the different stand age classes (n = 4) Age (years)
Sample locus
C
N
P
5
Above-ground mound Soil under mound Organic layer Mineral soil
25a 11 32,745 24,644
(8) (3) (5703) (2836)
0.5a (0.2) 0.5 (0.2) 1034 (183) 1170 (138)
0.04a (0.01) – 53 (9) –
30
Above-ground mound Soil under mound Organic layer Mineral soil
26a 14 25,074 23,499
(6) (3) (3438) (3452)
0.7 (0.1) 0.7 (0.2) 929 (153) 1179 (98)
0.05 (0.01) – 46 (3) –
60
Above-ground mound Soil under mound Organic layer Mineral soil
93 42 29,579 31,946
(49) (24) (4594) (7736)
2.1 (1.1) 2.0 (1.2) 933 (137) 1380 (337)
0.15 (0.09) – 43 (7) –
100
Above-ground mound Soil under mound Organic layer Mineral soil
180b 53 27,526 21,741
(63) (10) (2397) (5440)
3.7b (1.3) 2.6 (0.5) 817 (83) 997 (142)
0.25b (0.09) – 38 (3) –
Standard errors are in parentheses. Only the data indexed with different letters differ significantly ( p < 0.05) between stand age classes, only pools in ant mounds were tested.
the C/N ratio was higher in the ant mounds than in the organic layer in boreal coniferous and mixed forests in central Sweden (Lenoir et al., 2001), which implies that the material in the ant mounds was less decomposed than that in the surrounding organic layer. Low C/nutrient ratios usually indicate a fast decomposition rate (Berg and McClaugherty, 2003) but, for instance, N mineralization from decomposing litter can be associated with initially higher C/N ratios in mature forests than in clear-cut areas (Berg and Ekbohm, 1983). The ant mound material is selectively collected from the forest floor by ants, and in coniferous stands primarily consists of conifer needles. Norway spruce needle litter, which is common mound-building material, usually has lower N and P concentrations (Berg and Tamm, 1991; Johansson, 1995; Lundmark-Thelin and Johansson, 1997; Berg et al., 2000) than the ant mound material (Zakharov et al., 1981; Lenoir et al., 2001; Frouz et al., 2005; Risch et al., 2005), and therefore the presence of other ant mound material explains the higher nutrient concentrations. Ant mounds contain relatively more resin particles (Lenoir et al., 1999) and food remains than the surrounding organic layer. The soil microbe (Frouz et al., 1997; Laakso and Seta¨la¨, 1998) and root composition (Farji-Brener,
2000; Ohashi et al., in press) of ant mounds also differ from those in the surrounding soil, and they may have an impact on the C and nutrient concentrations. In a temperate forest in the Czech Republic, a higher N fixing bacterial assemblage was found in the ant mounds compared to the surrounding organic layer (Frouz et al., 1997). However, this was probably not the case in our study because the N concentrations were similar in the ant mounds and in the surrounding organic layer. Laakso and Seta¨la¨ (1998) found a larger soil animal biomass, suggesting a higher amount of resources, in ant mounds than in the surrounding forest soil in Finland, but no differences in the N and P concentrations between the surface layers of ant mounds and the surrounding litter layer. Fine root N and P concentrations were higher in ant mounds than in the surrounding organic layer (Ohashi et al., in press). Ants themselves have also been reported to affect litter quality (Stadler et al., 2006). Furthermore, the organic layer comprises the whole decomposition continuum from litter to humus, while the material in the ant mounds is less decomposed and younger. The higher C, N and extractable P concentrations in the soil under the ant mounds compared to the surrounding mineral soil might be explained by the input of organic material caused
Fig. 4 – Mean C/N ratios and their standard errors of ant mounds and surrounding organic layer, and soil under ant mounds and surrounding mineral soil in different stand age classes (n = 4). Only the data indexed with different lowercases and capitals differ significantly ( p < 0.05) between sample loci and between age classes, respectively.
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by the mixing activity of the ants, whilst nutrient leaching by percolation water is highly unlikely in the dry conditions of ant mounds. Also in Denmark, higher C, N (Kristiansen and Amelung, 2001) and P (Kristiansen et al., 2001) concentrations were found under the abandoned ant mounds than in the surrounding soil. Our results did not support the hypothesis that the nutrient concentrations would decrease in ant mounds simultaneously with the decreases in the surrounding soil during forest succession. In our study, nutrient concentrations in the organic layer did not decrease during forest succession, which was the opposite of earlier findings in boreal forests in southern Finland (Tamminen, 1991). Actually the C concentrations in the ant mounds increased slightly along with increasing stand age. The bulk densities of the ant mounds in subalpine forests in Switzerland (Risch et al., 2005) were similar to our values. The bulk densities in the above- and below-ground parts of the ant mounds were lower than in the surrounding soil. The interior of the mounds of the Formica rufa group is known to have a porous structure with ant tunnels and chambers, and the mineral soil under the mounds is also mixed with organic matter by the ants, resulting in a lower bulk density. There were no significant stand-age related differences in the bulk densities of the ant mounds although the bulk density seemed to be highest in the seedling stands. This might indicate reduced ant activity in the recently clear-cut sites, which leads to accelerated decomposition. The contribution of ant mounds to the total C, N and P pools in the forest soil was small (<1%), and smaller than that in the subalpine forests in Switzerland where it was 0.6–5% of the C and N pools in organic layer depending on the forest type (Risch et al., 2005). The pools in ant mounds may seem negligible when extrapolated to the ecosystem level. However, ant mounds were shown to increase the spatial heterogeneity in the distribution of C, N and P in forest soil, and this might also affect e.g. nutrient availability to the trees. The results of this study also show that more nutrients are accumulated in ant mounds along with forest succession.
Acknowledgements We acknowledge the technical help of Ms. Laura Ikonen, Mr. Teuvo Vauhkala, Ms. Anita Pussinen, Ms. Seija Repo, Ms. Anki Geddala, Dr. Sirpa Piirainen and Ms. Maini Mononen. We thank Mr. Pekka Punttila for identification of the ant species and Mr. Jaakko Heinonen for statistical advice. Thanks go to Dr. John Derome for revising the text. We appreciate the comments of two anonymous reviewers. The Academy of Finland (project 200870) financed the study.
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