Does the mutualism between wood ants (Formica rufa group) and Cinara aphids affect Norway spruce growth?
Introduction
Many ant species have mutualistic relationships with aphids feeding on the phloem sap of a wide variety of plants (e.g. Way, 1963, Buckley, 1987, Stadler and Dixon, 2005, Styrsky and Eubanks, 2007). Wood ants (Formica rufa group) protect aphids from predators, and in return, are supplied with honeydew excreted by aphids. Ants may collect more than 80% of the excreted honeydew (Douglas and Sudd, 1978), which constitutes 62–94% of their diet (Wellenstein, 1952, Rosengren and Sundström, 1991). Honeydew contains 15–20% sugars and a small amino acid component (Zoebelein, 1956a, Stradling, 1987, Rosengren and Sundström, 1991). A wood ant colony can bring 240–1000 kg of honeydew (fresh weight) annually to its mound (Zoebelein, 1956b, Wellenstein, 1980, Stradling, 1987, Rosengren and Sundström, 1991). Simultaneously, wood ants prey on a large number of other arthropods (Way and Khoo, 1992, Martikainen et al., 2000, Punttila et al., 2004). Ants may predate on other arthropods more intensively in mutualistic relationships with aphids than otherwise (Way, 1963), which would also benefit the tree as defoliating insects are removed.
The removal of carbohydrates from the phloem by aphids can reduce tree growth. The net effect of ant–aphid mutualism on tree growth is the difference between the direct loss caused by sap sucking and the indirect positive effect due to ants removing non-tended herbivores. The net effect of ant–aphid mutualism on tree growth is likely to be positive when the populations of leaf-defoliators are high, while ant predation on low populations does not compensate for the sap removal (e.g. Styrsky and Eubanks, 2007). Usually the growth of deciduous trees responds positively to wood ant–aphid mutualism (e.g. Whittaker and Warrington, 1985, Sipura, 2002), but not always (e.g. Dixon, 1971, Sipura, 2002). In contrast, wood ant–aphid mutualism has been shown to suppress the growth of Scots pine in several studies (Klimetzek and Wellenstein, 1978, Wellenstein, 1980, Rosengren and Sundström, 1991). Unlike deciduous trees, conifers have few defoliating insects, which seldom cause severe canopy damage and consequent growth reduction in Fennoscandia. Thus, the ant–aphid mutualism is likely to have a negative net effect on the growth of conifers.
Many studies have shown that timber harvesting by clear-cutting is detrimental to wood ants by reducing food resources, disrupting orientation, and changing micro-climate. However, wood ant populations recover or re-colonize as a new forest stand develops (Punttila et al., 1991, Punttila, 1996, Sorvari and Hakkarainen, 2007, Kilpeläinen et al., 2008). Thus, the impact of wood ants on tree and stand growth may vary with stand age. Here we studied for the first time the effect of wood ant–aphid mutualism on Norway spruce by measuring growth on both the tree and the ecosystem level, in forest stands of different age (cf. Laakso and Setälä, 2000, Frouz et al., 2008), and by experimentally manipulating the wood ant–aphid mutualism (Styrsky and Eubanks, 2007). We base our main conclusions on the results of this experiment but also present correlative results for comparison with earlier studies. Therefore, the objective of our study was to assess the effect of mutualism between wood ants (Formica rufa group) and aphids (Cinara spp.) on the growth of Norway spruce in stands of different ages.
Section snippets
Study areas
The study was conducted in four replicate 5-, 30-, 60- and 100-year-old stands (2.3–11.3 ha) growing on medium-fertile Myrtillus-type (Cajander, 1949) sites in eastern Finland (29°52′E, 63°04′N, 160 m a.s.l.). The 16 stands were dominated by Norway spruce (Picea abies (L.) Karst.), and contained an admixture of Scots pine (Pinus sylvestris L.) and some deciduous tree species (Table 1). The number (Table 2) and the location of wood ant mounds in these stands were known from a previous study (
Tree height and radial growth—tree level
In the 5-year-old stands the height growth of heavily visited seedlings was 16.3% higher than in the seedlings with ant traffic blocked (Fig. 1), but the difference was not significant (P = 0.100, “block contrast”, Table 4). In the 30-year-old stands, the radial growth of heavily visited trees was 7.3% lower than for trees where ant traffic was blocked (P = 0.013) (Table 4, Fig. 1). In the older stands, the radial growth of the trees that were heavily visited before the experiment was ca 6% lower
Discussion
Ant–aphid mutualisms can have both negative and positive effects on tree growth (Styrsky and Eubanks, 2007), and for instance the chemical defence of the host plant (Sipura, 2002), birds (Mooney and Linhart, 2006, Mooney, 2007), aphid saliva (Miles, 1999) and aphid-transmitted plant viruses (Ng and Perry, 2004, Goggin, 2007) interact with the effect. Here we studied the total net effect of ant–aphid mutualism on the stem growth of Norway spruce, and based our main results on a manipulative
Conclusions
We found that wood ant–aphid mutualism was associated with a clear positive but non-significant height growth response in individual 5-year-old Norway spruce seedlings, but had a significant negative effect on the stem growth of individual fast-growing 30-year-old Norway spruces. The growth reduction may last several years in mature spruces. However, growth responses at the stand level were negligible, because only a small number of trees are heavily visited. Nonetheless wood ants increase
Acknowledgements
We thank the field and laboratory staff of the Finnish Forest Research Institute, Joensuu Research Unit and the University of Joensuu, Faculty of Forest Sciences for helping in data collection. We are grateful to Mr. Pekka Punttila for ant species identification, to Dr. Anders Albrecht for aphid species identification, to Mr. Jaakko Heinonen for statistical advice, and to Prof. Heikki Setälä and two anonymous reviewers for constructive comments on the manuscript. The Academy of Finland
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