Dicamba drift alters plant–herbivore interactions at the agro‐ecological interface

Abstract

Natural populations evolve in response to biotic and abiotic changes in their environment, which shape species interactions and ecosystem dynamics. Agricultural systems can introduce novel conditions via herbicide exposure to non‐crop habitats in surrounding fields. While herbicide drift is known to produce a variety of toxic effects in plants, little is known about its impact on nontarget wildlife species interactions. In a two‐year study, we investigated the impact of herbicide drift on plant–herbivore interactions with common weed velvetleaf (Abutlion theophrasti) as the focal species. The findings reveal a significant increase in the phloem‐feeding silverleaf whitefly (Bermisia tabaci) abundance on plants exposed to herbicide at drift rates of 0.5% and 1% of the field dose. We also identified a significant phenotypic trade‐off between whitefly resistance and herbicide resistance in addition to whitefly resistance and relative growth rate in the presence of dicamba drift after increasing the populations grown in Year 2. In a follow‐up greenhouse study, we found evidence that dicamba drift at 0.5% of the field dose significantly increased the average chlorophyll content (in milligrams per square centimeter) along with a positive correlation between whitefly abundance and chlorophyll content. Overall, these findings suggest herbicide exposure to nontarget communities can significantly alter herbivore populations, potentially impacting biodiversity and community dynamics of weed populations found at the agro‐ecological interface.

The consequences of synthetic auxin herbicide on plant-herbivore interactions

“…However, also in rice, larvae of a moth stem borer grew better when plants were sprayed with 2,4-D as a result of higher nitrogen content in the plants [59], and in two separate field experiments, the abundance of whitefly larvae (a sap-sucking insect) increased on velvetleaf plants exposed to dicamba drift (0.5 and 1% of the field dose [17]). These results suggest that because of synthetic auxin exposure, either lowered defenses or altered nutrients in plants can induce herbivory in some species and field contexts.…”

“…If the addition of synthetic auxin at drift doses leads to deregulation of normal herbivory responses, we would expect to find a higher rate of herbivory among plants exposed to dicamba drift. There is evidence for increased herbivory in the presence of dicamba in some species [17,43], but whether this is due to the suppression of normal herbivory defense pathways is currently unknown. Because auxins are crucial phytohormones that regulate a host of plant processes at different times in plant development [31], there are many potential effects from exposure to synthetic auxins at drift doseswhether phenotypic or occurring at the biochemical level -and any number of these alterations could underlie changes in herbivore pressure in the presence of drift.…”

“…Affected plants can also show reduced height and yield reduction, the latter depending on the timing of exposure and other environmental conditions [15,44,47,48]. We have comparatively less information on the direct effects of synthetic auxin drift on natural weeds [49], but the phenotypic effects have been described as reduced size and/or height [16,50], greater number of small leaves, leaf cupping, and greener leaves (i.e., increased chlorophyll content in velvetleaf [17]). A study of common weed species in the greenhouse [51] exposed to dicamba drift at 1% the field dose finds similar phenotypes -i.e., leaf cupping, reduced size -but strikingly, finds wide variation in species' damage, biomass, and growth responses, with some species showing leaf damage and reductions in biomass (Ipomoea hederacea, Solidago canadensis, Persicaria pensylvanica, Daucus carota, Amaranthus palmeri, Trifolium pratense) whereas others showing limited effects, or even little leaf damage and/or evidence of increased size (Physalis philadelphica, Plantago virginica, Sida spinosa).…”

“…We consider flowering patterns here since florivorous insectsherbivores that feed on floral parts including nectar robbing -could likewise be impacted (Fig 2B). In response to dicamba drift, weedy species can display delayed flowering and/or reduced flower number [17,19,50], a response that is common but not ubiquitous across species [51]. A survey of natural weed communities exposed to low doses of dicamba (1% the field dose) showed a reduction in the abundance and flowering of forbs, but no alteration of overall floral resources within a community, presumably because less-sensitive broadleaved species were able to flower despite the reduction in forb cover [19].…”

“…However, herbicide use can lead to unintentional outcomes -namely, herbicide resistance [10], changes to weed community structure [11,12], and herbicide drift, defined as the exposure of nontarget areas to low doses of herbicide (i.e., ~1-5% of the field dose, [13]). Although drift levels of herbicide are typically well below the threshold for immediate toxicity, exposure to drift can still cause significant plant damage [14][15][16][17]. While we have some information on the effect of drift on crop species [18], our knowledge of how drift may impact natural plant communities and the important plant-insect interactions that occur within them is strikingly limited [19,20].…”