Plasticity in within-plant distribution patterns allows aphids to optimize their fitness under contrasting interactions with protective ants and predatory ladybugs

Phenotypic plasticity is a crucial adaptive strategy that allows organisms to respond to environmental changes. Many aphids have evolved mutualistic relationships with ants, whereby aphids provide honeydew in exchange for protection from natural enemies. Such ant–aphid mutualisms are often facultative and aphid colonies must often cope without ants. We show here that attendance by red imported fire ants, Solenopsis invicta, alters the within-plant distribution of cotton aphids (Aphis gossypii), resulting in fewer aphids on leaves and more on the stem, petioles, and sprouts (SPS) of cotton seedlings compared to colonies without ant attendance. The nitrogen contents in stems and sprouts were higher than in leaves, which may be a reason for the significantly higher population growth in ant-tended colonies. In contrast, exposure to the signals of a predatory ladybug, Coccinella septempunctata, resulted in a remarkably smaller aphid colony size, with lower proportions of aphids distributed on SPS, but a higher proportion on the leaves, compared to those in the predator-free colonies. In addition, ladybug predation risk is considerably higher on SPS than on leaves, and aphids showed rapid positional shifts from stems to leaves upon direct exposure to a ladybug, highlighting their ability to respond swiftly to predator presence. Our findings reveal that adaptive plasticity in aphid distribution patterns enables aphid colonies to optimize their fitness by responding to the presence of mutualistic ants or predatory threats with flexibility.