Complex Effects of Fertilization on Plant and Herbivore Performance in the Presence of a Plant Competitor and Activated Carbon

<div><p>Plant-herbivore interactions are influenced by host plant quality which in turn is affected by plant growth conditions. Competition is the major biotic and nutrient availability a major abiotic component of a plant’s growth environment. Yet, surprisingly few studies have investigated impacts of competition and nutrient availability on herbivore performance and reciprocal herbivore effects on plants. We studied growth of the specialist aphid, <i>Macrosiphoniella tanacetaria</i>, and its host plant tansy, <i>Tanacetum vulgare</i>, under experimental addition of inorganic and organic fertilizer crossed with competition by goldenrod, <i>Solidago canadensis</i>. Because of evidence that competition by goldenrod is mediated by allelopathic compounds, we also added a treatment with activated carbon. Results showed that fertilization increased, and competition with goldenrod decreased, plant biomass, but this was likely mediated by resource competition. There was no evidence from the activated carbon treatment that allelopathy played a role which instead had a fertilizing effect. Aphid performance increased with higher plant biomass and depended on plant growth conditions, with fertilization and AC increasing, and plant competition decreasing aphid numbers. Feedbacks of aphids on plant performance interacted with plant growth conditions in complex ways depending on the relative magnitude of the effects on plant biomass and aphid numbers. In the basic fertilization treatment, tansy plants profited from increased nutrient availability by accumulating more biomass than they lost due to an increased number of aphids under fertilization. When adding additional fertilizer, aphid numbers increased so high that tansy plants suffered and showed reduced biomass compared with controls without aphids. Thus, the ecological cost of an infestation with aphids depends on the balance of effects of growth conditions on plant and herbivore performance. These results emphasize the importance to investigate both perspectives in plant herbivore interactions and characterize the effects of growth conditions on plant and herbivore performance and their respective feedbacks.</p></div

Dependence of plant biomass log response ratio on aphid numbers.

<p>Tansy plant biomass LogRR was measured as tansy biomass in the presence of aphids (<i>Macrosiphoniella tanacetaria</i>) divided by control plant biomass. This analysis combined host plants of all additional treatments imposed in the experiment.</p

Results from linear mixed-effects models for plant and aphid performance as depending on host plant growth conditions.

<p>Given are separate models for tansy biomass, the log response ratio (plant biomass LogRR) of tansy biomass infested with aphids compared with control plants, aphid numbers, and aphid load (aphid number per unit plant biomass) from a greenhouse experiment using <i>Macrosiphoniella tanacetaria</i> on <i>Tanacetum vulgare</i> in competition with <i>Solidago canadensis</i>. Minimum adequate models are presented together with terms removed from the model given in brackets. Superscripts give the order in which terms have been removed from the model starting with highest order interactions based on least significance. Significant terms in the final models are given in bold. A random effect for 5 blocks which was included in all models is not shown. °In the model for tansy biomass, aphid presence (AP) was included as explanatory variable, while in the model for aphid number, tansy biomass (TB) was used as a covariate. The biomass of the control plants not infected with aphids but exposed to the same other treatments was used as covariate because this biomass was not confounded with the aphid effect of reducing plant biomass. *indicates data was log transformed.</p

Dependence of aphid numbers on the biomass of the host plant.

<p>Open circles and dashed line represent the number of <i>Macrosiphoniella tanacetaria</i> aphids on tansy plants in soil without activated carbon. Closed circles and solid line are aphid numbers on plants in soil treated with activated carbon. The biomass of the control plants not infected with aphids but exposed to the same other treatments was used as explanatory variable because this biomass represents the potential size of the plants without the reduction of plant size due to the aphid infection.</p

Response of plant and aphid performance on host plant growth conditions.

<p>Tansy growth conditions were manipulated in experimental treatments with three levels of fertilizer crossed with two levels of activated carbon (AC), competition and infestation with aphids (<i>Macrosiphoniella tanacetaria</i>). We replicated every treatment combination 5 times, yielding a total of 2×2×3×2×5 = 120 pots. (A) tansy biomass, (B) plant biomass log response ratio (plant biomass LogRR), i.e. biomass of plants infested with aphids divided by biomass of control plants subjected to the same fertilization, AC and competition treatment, (C) aphid number, and (D) aphid load (aphid number per unit plant biomass). The colour of bars indicates aphid treatment (black bars: with aphids, gray bars: without aphids) while bar patterns indicate the AC treatment (+AC: black and hatched columns; −AC: white and slanted columns) and the competition treatment (with competition (+C): hatched and slanted and without competition (−C): white and black columns). Means ± SE are shown. For statistical tests see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103731#pone-0103731-t001" target="_blank">Table 1</a>.</p