Costs and benefits of ant attendance to the drepanosiphid aphid Tuberculatus quercicola

Abstract

The defensive effects of ants against aphid predators have been well documented in the mutualistic relationship of aphids and their attending ants. However, it is not clear whether ant attendance has any direct effect on the aphids’ growth and reproduction. Through field experiments, this study evaluates the benefits and, in particular, the costs of ant attendance to aphid colonies, focusing on the drepanosiphid aphid Tuberculatus quercicola which is associated with the Daimyo oak, Quercus dentata, and which is always attended by the red wood ant Formica yessensis. Ant attendance was clearly beneficial to the aphid; the exclusion of ants led to a significant increase in the extinction rate of aphid colonies. However, MANOVA and randomized block ANOVA indicated that in colonies continuously attended by ants, aphids had significantly smaller body size and produced a smaller number of embryos than in colonies isolated from ants when they were reared under homogeneous host conditions free from natural enemies. Thus, ant attendance had a negative influence on the growth and reproduction of the aphids, even though it contributed to the greater longevity of the aphid colonies. We hypothesize that ant‐attended aphids are under intense selective pressures that act against aphid clones which fail to attract many ants, so that aphids have developed an adaptive mechanism to allocate a larger fraction of resources to the honeydew when they are requested to do so by the ants in order to ensure the ants’ consistent visitation.

The degree of protection different ants (Hymenoptera: Formicidae) provide aphids (Hemiptera: Aphididae) against aphidophages

“…Ants collect sugar-rich excretions of trophobionts (honeydew) and in exchange protect them from their natural enemies (e.g. Way, 1963;Vepsäläinen & Savoläinen, 1994;Yao et al, 2000;Fischer et al, 2001). Ants are known to have trophobiotic relationships with insects of three orders: Hemiptera, including insects of three suborders: Sternorrhyncha (aphids, scale insects, white flies), Auchenorrhyncha (leafhoppers, planthoppers) (Delabie, 2001) and Heteroptera (true bugs) (Gibernau & Dejean, 2001;Waldkircher et al, 2004), Lepidoptera (larvae of Lycaenidae, Riodinidae and Tortricidae) (Maschwitz et al, 1986;Pierce et al, 2002) and Hymenoptera (larvae of the sawfly Blasticotoma filiceti Klug) (Shcherbakov, 2006;Novgorodova & Biryukova, 2011a).…”

The Origin of a Mutualism: A Morphological Trait Promoting the Evolution of Ant-Aphid Mutualisms

“…In particular, tended aphids increase the honeydew concentration of melezitose, a trisacharide particularly attractive to ants (Fischer and Shingleton 2001). There is evidence that such adjustments incur costs to the aphids (Stadler and Dixon 1998;Yao et al 2000), which are likely to increase if there is competition between aphid species for ant partners. We suggest that only in species feeding on deeper phloem elements will the costs of these traits be outweighed by the benefits of protection from predators.…”

Costs and constraints in aphid‐ant mutualism

“…For instance, the ant Formica yessensis Forel caused the rate of honeydew excretion by the aphid Tuberculatus quercicola (Matsumura) to increase twofold compared to the ant-exclusion treatment. In this case, ant attendance led to the poor assimilation of phloem sap, along with a decrease in the body size of the aphids and the number of embryos (Yao et al 2000;Akimoto 2001, 2002). In the mutualism between Aphis craccivora Koch and L. niger, the ants suppressed the development of the aphid colony (Katayama and Suzuki 2002), probably due to an increase in honeydew excretion (Takeda et al 1982).…”