María Natalia Lescano: The complex role of bottom-up cascading effects: Excess nutrients make aphids less attractive to mutualistic ants

In our latest post, María Natalia Lescano, researcher at CONICET and University of Comahue, discusses their paper ‘Excessive nutrient input induces an ecological cost for aphids by modifying their attractiveness towards mutualist ants, whilst also showcasing their fantastic tri-trophic study system and discussing the importance of cascading effects in ecosystems.

About the paper

Ecological stoichiometry considers the balance of energy and elements on organisms and how this balance affects biotic interactions. This is based on the premise that carbon (C), nitrogen (N) and phosphorus (P) are three of the main constituents of structural biological molecules, meaning  the balance among their relative proportions determines biological functions such as growth and reproduction. Plants are usually poor in nutrients (i.e., they have high C:N:P ratios) and their  elemental composition is influenced by soil nutrient availability. On the other hand, animals can regulate their stoichiometry despite elemental variations in their food (i.e., they possess stoichiometric homeostasis) and demand large amounts of N and P to maintain their vital functions. Consequently, the largest elemental imbalances are found at the bottom of trophic chains, decreasing in importance whilst moving through higher trophic levels.

Herbivores need to use different mechanisms to compensate for the low quality of their diet, which demand energy and restrict their performance. However, plants growing in soil with excessive nutrients can also become unbalanced via a low C:N:P ratio. When plant N and/or P are in excess, herbivores also need to expend energy associated with the energetic and toxicity costs of metabolizing them, which also limits their performance. This has led to the proposal of the stoichiometric knife-edge hypothesis, which postulates that the performance of herbivores decreases if the imbalance involves insufficient (very high C:N:P ratio) or excess (very low C:N:P) nutrient content. As a consequence, changes in soil nutrient availability, by modifying the C:N:P ratio of plants and affecting herbivores, may also have consequences that scale up to higher trophic levels (e.g., natural enemies or mutualists).

Thistles growing in Northwestern Patagonian steppe, Argentina. (credit: María Natalia Lescano)

Plant-aphid-ant interactions are an amazing and ideal terrestrial system to study whether different availability of soil N— by altering the C:N ratio of plants— directly modifies herbivore performance and/or indirectly impacts on higher trophic levels. Aphids are herbivores particularly specialized in low nutrient foods (phloem feeders), and one adaptation to this poor-quality diet is eating large amounts of sap to obtain adequate amounts of nutrients; this results in an excess of carbohydrates, certain amino acids, and water that are excreted in the form of honeydew. The honeydew is a valuable food resource for ants, and in exchange for it, ants actively protect aphids from predators and parasitoids. The quantity and quality of honeydew determine the degree of ant attraction to a host plant with aphids, which leads to greater numbers of ants patrolling and may also benefit aphid performance. Thus, changes in soil nutrients, by modulating the C:N balance of plants and affecting aphids and honeydew production, may determine the attraction of aphid-tending ants, modulating the dynamics of ant-aphid relationships and affecting the arthropod communities on plants.

Soil fertilization occurs naturally in several ecosystems, for example, where nutrient-poor soils are enriched by the presence of “fertility islands” generated by the activity of animals that modify soil resources, or due to natural spatial variability in soil composition. Furthermore, human activities have strongly altered the biogeochemical cycles of key elements, such as C, N, and P via nutrient enrichment. So, documenting the existence of a stoichiometric knife-edge at terrestrial ecosystems, as well as how the changes at the base of a food chain can spread upwards and affect organisms in all trophic levels, becomes particularly important.

About the research

Our study assessed how the enhancement of soil nutrient availability affects (1) host plant tissue quality (C: N ratios), (2) aphid physiological responses (honeydew production and composition and aphid body elemental balance) and population growth, and (3) the attraction of mutualistic ants towards aphid-infested plants. In Northwestern Patagonia, Argentina, we performed a common garden experiment with thistle, aphids and aphid-tending ants under three increasing fertilization levels (i.e., control treatment: unfertilized nutrient-poor soils from the Patagonian steppe; NPK-rich soil: soil enriched with 1 dose of fertilizer; and 2NPK-rich soil: soil enriched with 2 doses of fertilizer).

Study system: thistle, aphid and aphid-tending ants. (credit: María Natalia Lescano)

We found that fertilized soils increased the biomass and reduced the C:N ratio of thistles, and also increased aphid abundance. Despite the huge reduction in the C:N ratio of thistles with increased soil nutrients, aphids were able to maintain their body nutrient balance (they regulated their internal elemental composition, known as stoichiometric homeostasis)— this was possible through changes in honeydew production and composition!!!! Fertilization treatments led to a reduction by half (or even more) in the quantity of honeydew secreted and a large increase in honeydew N concentration compared with unfertilized treatment.

The final phase experiment in the greenhouse (credit: María Natalia Lescano)

But more is not always better… The N-enriched honeydew secreted by aphids from extra fertilized plants was partly due to an increase in the content of uric acid (a waste toxic compound). This could explain that aphid-tending ants have a marked preference for honeydew from intermediate rich-substrates (i.e., honeydew with a lower C:N ratio compared to unfertilized plants, and lower uric acid compared with 2NPK-rich plants) and, thus, why the aphid-infested thistles had the highest number of aphid-tending ants when they grew on intermediate rich-substrates. The highest fertilization used here was neither deleterious for aphids, nor represented a benefit to them in terms of performance compared with intermediate fertilization. Nevertheless, a disproportionate increase in fertilization could imply an ecological cost due to the decrease in the attraction of protective mutualists. Fewer ants patrolling a plant may represent a higher vulnerability of aphids to natural enemies because it diminishes the chances of ants to kill or expel aphid enemies, inducing an ecological cost.

Thus, our study provides key insights into the complex role of bottom-up, cascading effects triggered by increases in soil nutrient availability, and highlights the importance of evaluating not only the physiological and population costs/ benefits of it, but also the ecological ones; especially when it alters mutualistic interactions.

About the author

María Natalia Lescano in one of Bariloche’s many landscapes

I am curious and passionate about nature. I live in Bariloche, Argentina— an ideal place for a biologist! I enjoy answering questions of conceptual interest on topics of ecology and behavior, with emphasis on those processes that involve ants. My PhD was focused on the direct and indirect effects of enhanced soil nutrient availability generated by the leaf-cutting ants, Acromyrmex lobicornis, on the food chain composed of plants, aphids, tending ants, and aphid natural enemies.

Currently, I am a CONICET adjunct researcher at the Laboratorio de Investigaciones en Hormigas, INIBIOMA (CONICET-UNCo), and assistant teacher at Universidad Nacional del Comahue. My research interests focus on understanding how nutritional imbalances at the base of trophic chains impact on the dynamics of animal-plant interactions, with emphasis on mutualistic associations. Within the topic of nutritional ecology, I am also interested in understanding whether different food components influence food choice, physiological regulation and fitness of ants, and how this modulates the role of ants in ecosystems.

Enjoyed the blogpost? Read the research here!

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