The potential effects of red imported fire ants (Solenopsis invicta) on arthropod abundance and Cucumber mosaic virus

Abstract

Mutualisms involving ants and honeydew-producing insects such as aphids, scales, and whiteflies may dramatically affect the population dynamics of these herbivorous insects. Furthermore, changes in the population size of honeydew-producing insects may have important consequences for other interacting organisms. We tested the hypothesis that ant-aphid mutualisms result in significant increases in aphid population size and aphid dispersal which, in turn, increases the spread of aphid-vectored plant viruses. We studied the invasive red imported fire ant (Solenopsis invicta), several common aphids that form facultative mutualisms with these ants, and a ubiquitous, aphid-vectored plant virus (Cucumber mosaic virus (CMV)). We found that aphids were significantly more abundant in small plots of tomato plants (Lycopersicon esculentum) with large fire ant populations than in small plots of tomato with suppressed fire ant populations. In a greenhouse experiment, we found that aphids dispersed to neighboring plants 59% more often in the presence of fire ants than in the absence of fire ants, suggesting that fire ants increase aphid movement. Most importantly, in a large-scale field study (˜ 2.4 hectare fields), we found that the abundance of alate aphids and the incidence of CMV (the proportion of plants infected with virus) were significantly higher in fields with high densities of fire ants than in fields with suppressed fire ant populations. This study suggests that ant-aphid mutualisms may have dramatic, previously undocumented effects on the dynamics of aphid-vectored plant viruses. This study also suggests that the continued range expansion of red imported fire ants could result in larger levels of virus infection in both agricultural crops and wild plants. Understanding epidemiology of plant viruses requires knowledge of their ecology and hosts. Identifying reservoir hosts and inoculum sources of plant viruses is often imperative for understanding virus outbreaks in agricultural plants. We present here a 2-year analysis of the population dynamics of Cucumber mosaic virus (CMV) in herbaceous plants around fresh-market tomato fields in northern Alabama, a region where a persistent CMV epidemic has been ongoing for over ten years. Over the two year study, at least 50 herbaceous plant species belonging to 27 families were identified and tested for the presence of CMV. 18 plant species belonging to 12 plant families tested positive for CMV. In 2005, CMV incidence was positively correlated with planting date of the field for both tomato and herbaceous plants. There was no correlation between the overall CMV incidence in weed plots and CMV incidence in neighboring tomato fields, but there were strong, positive correlations between CMV incidence in tomato fields and the relative abundance of greenbriar (Smilax spp.), the relative abundance of ivy-leaf morningglory (Ipomoea hederacea), the abundance of aphids on ivy-leaf morningglory, and the number of aphids on blackberry (Rubus spp.). These results suggest that most herbaceous plants near Alabama tomato fields are relatively unimportant in the spread of CMV to neighboring tomato fields and that control efforts should be focused on only a handful of species.