Does the mutualism between wood ants (Formica rufa group) and Cinara aphids affect Norway spruce growth?

Abstract

Ant–aphid mutualisms, in which ants tend aphids, which in turn provide honeydew to the ants, are widespread and have been shown to affect plant growth. In boreal forests the effect of ant–aphid mutualism on tree growth can vary with stand age, because forest clear-cutting harms the ecologically most dominant ant partner in such mutualisms, wood ants (Formica rufa group). We studied whether the mutualism between wood ants and Cinara aphids affects the growth of boreal Norway spruces (Picea abies L. Karst.) in stands of different ages. In boreal forests, conifers, unlike deciduous trees, have only few defoliating insects, and therefore we expected the growth loss of conifers due to sap sucking by aphids not to be compensated by reduced insect herbivory due to predation by wood ants. The study was conducted in medium-fertile spruce-dominated stands in eastern Finland. We used stands of four different age classes (5, 30, 60 and 100 years) and selected ten spruces heavily visited and ten spruces lightly visited by ants around five medium-sized ant mounds in each stand age class. The access of ants was blocked on half of the trees in both groups. In the 5-year-old stands, the mean annual height growth of individual heavily visited seedlings was 16.3% greater than in the ones where ant traffic was blocked, but this difference was not significant. In the 30-year-old stands, the mean annual radial growth of the heavily visited spruces was 7.3% smaller than in trees where ant traffic was blocked, and this difference was significant. The mutualism had no significant effect on the radial growth in the 60- and 100-year-old stands. In the 60-year-old stands, however, the spruces that were visited heavily prior to the beginning of the study grew significantly less relative to their past growth than the initially lightly visited trees during the study. This suggests that the ant–aphid mutualism may have long-term effects on tree growth. The ant–aphid mutualism had no significant effect on the growth at the stand level. The results indicate that ant–aphid mutualism can have a significant effect on the growth of individual spruces, but the effect is negligible at ecosystem level.

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.