Excessive nutrient input induces an ecological cost for aphids by modifying their attractiveness towards mutualist ants

LESCANO, M. N.; QUINTERO, C.; FARJI BRENER, A. G.; BALSEIRO, E.

FUNCTIONAL ECOLOGY

WILEY-BLACKWELL PUBLISHING, INC

Año: 2022

0269-8463

1. Enhanced soil nutrient availability often favors herbivore performance by bringing thecarbon:nutrient ratio of plants closer to herbivore requirements. However, a surplus ofnutrients can promote a too low carbon:nutrient ratio in plants, making them of poorquality for herbivores. In addition, increased soil nutrients can trigger cascadingeffects altering higher trophic levels, resulting in indirect costs for herbivores.2. Through experiments under three increasing fertilization levels (unfertilized, NPKrich,and 2NPK-rich soils), we studied how the enhancement of soil nutrientavailability, by modifying the C:N ratio of thistles, affects the performance andhomeostatic response of the aphids, and the consequent ant attraction.3. Fertilized soils increased the biomass and reduced the C:N ratio of thistles, alsoincreasing aphid abundance. The stoichiometric homeostasis of aphids was modulatedthrough changes in honeydew production and composition; fertilization treatmentsreduced by more than half the quantity of honeydew secreted and lead to 2.5 to 6.4times higher honeydew N concentration compared with the unfertilized treatment. Inaddition, in the highest fertilization treatment, the aphids increased the content of uricacid (a waste toxic compound involved in amino acid deamination) excreted in theirhoneydew. Aphid-infested thistles had the highest number of aphid-tending ants whenthey grew on intermediate rich-substrates. Ants selected honeydew with a lower C:Nratio (compared to unfertilized plants), but fewer workers patrolled plants with thehighest fertilization treatment likely due to increased uric acid in the honeydew.4. We showed that enhanced soil nutrients brought plant C:N ratio closer to aphidrequirements, enhancing their performance and promoting ant attendance. But adisproportionate increase in fertilization did not further improve aphid performancewhile it decreases the attraction of protective ants, which would make aphidpopulations more vulnerable to attack by natural enemies, inducing an ecological cost.5. This study highlights the complex role of bottom-up cascading effects triggered byincreases in soil nutrient availability and the importance of evaluating not only thephysiological and population cost and benefits of it but also the ecological ones;especially when it alters mutualistic interactions.