Within-Plant Bottom-Up Effects Mediate Non-Consumptive Impacts of Top-Down Control of Soybean Aphids

Abstract

There is increasing evidence that top-down controls have strong non-consumptive effects on herbivore populations. However, little is known about how these non-consumptive effects relate to bottom-up influences. Using a series of field trials, we tested how changes in top-down and bottom-up controls at the within-plant scale interact to increase herbivore suppression. In the first experiment, we manipulated access of natural populations of predators (primarily lady beetles) to controlled numbers of A. glycines on upper (i.e. vigorous-growing) versus lower (i.e. slow-growing) soybean nodes and under contrasting plant ages. In a second experiment, we measured aphid dispersion in response to predation. Bottom-up and top-down controls had additive effects on A. glycines population growth. Plant age and within-plant quality had significant bottom-up effects on aphid size and population growth. However, top-down control was the dominant force suppressing aphid population growth, and completely counteracted bottom-up effects at the plant and within-plant scales. The intensity of predation was higher on upper than lower soybean nodes, and resulted in a non-consumptive reduction in aphid population growth because most of the surviving aphids were located on lower plant nodes, where rates of increase were reduced. No effects of predation on aphid dispersal among plants were detected, suggesting an absence of predator avoidance behavior by A. glycines. Our results revealed significant non-consumptive predator impacts on aphids due to the asymmetric intensity of predation at the within-plant scale, suggesting that low numbers of predators are highly effective at suppressing aphid populations.

Non-additive effects of simulated heat waves and predators on prey phenotype and transgenerational phenotypic plasticity

“…In the presence of predators, the aphid's spatial distribution significantly shifted towards the lower leaves of the plants. Because coccinellids tend to forage more often and longer on the plant's upper parts (Costamagna & Landis, ; Hodek & Honĕk, ), we attribute this spatial distribution shift to a predator avoidance behaviour that, as reported in previous studies, reduces predation risk at the cost of feeding on lower‐quality plant tissues (Costamagna & Landis, ; Costamagna et al., ).…”

“…This reduces the immediate predation risk at a cost of garnering resources in suboptimal environments (Downes, ; Lima, ; Sih, Englund, & Wooster, ). Here, we found that, in the absence of ladybeetles, aphids typically stay at the plant's apex, which is their preferred feeding site due to the high nutritional quality of vigorously growing apical tissues (Cibils‐Stewart, Sandercock, & McCornack, ; Cornelissen, Wilson Fernandes, & Vasconcellos‐Neto, ; Costamagna, McCornack, & Ragsdale, ; Dixon, ). In the presence of predators, the aphid's spatial distribution significantly shifted towards the lower leaves of the plants.…”

Effects of crowding and host plant quality on morph determination in the soybean aphid,Aphis glycines

“…Aphis glycines performance is positively correlated with G. max N content (Myers et al., ; Myers & Gratton, ; Walter & DiFonzo, ), which is highest in the top nodes (Muchow et al., ; Shiraiwa & Sinclair, ). Although the within‐plant distribution of A. glycines changes throughout the season, most individuals in a colony are typically found feeding on the top nodes of G. max (Wu et al., ; McCornack et al., ; Costamagna & Landis, ; Costamagna et al., ). Thus, the within‐plant spatial distribution of A. glycines likely constitutes a behavioral adaptation to within‐plant quality variation, as is observed in other aphid species (Dixon, ; Straw et al., ).…”

“…To achieve this, unifoliate leaves of G. max plants grown under laboratory conditions were excised and placed on moist paper towel circles kept inside plastic Petri dishes (1 cm high, 9 cm diameter; Fisherbrand, Ottawa, ON, Canada). Young G. max leaves were used due to their high nutritional quality, demonstrated by A. glycines aggregations on newly developed plant tissue (McCornack et al., ; Costamagna et al., ). Adult apterous aphids were haphazardly selected from the laboratory colony and placed in groups of three on the excised leaves, where they were allowed to reproduce for 24 h before being removed.…”

“…Similarly, previous plant infestations by conspecifics can result in increases or reductions in plant quality for aphids and other sap‐feeding insects (Denno et al., ; Awmack & Leather, ; Chiozza et al., ; Varenhorst et al., ). Finally, spatial variations in within‐plant quality can also affect the performance of aphids (Watt, ; Costamagna et al., ).…”