The goal of this project was to develop and disseminate a biological disease control strategy for potato growers that minimizes PVY spread by enhancing naturally occurring aphid natural enemy populations. To begin this work, a total of twenty-two farms were surveyed for aphids, aphid natural enemies, and PVY over two growing seasons (2012 and 2013), and the landscape composition of the area surrounding the farm was analyzed using ArcGIS software. In both 2012 and 2013, there was a significant positive relationship between the amount of agricultural land surrounding a farm and the end of season PVY prevalence on farms with infection; the more agriculture in the area, the more PVY there was. Our results also indicate that while ladybug predators have an effect on disease prevalence, the relationship between landscape composition and PVY prevalence is most likely mediated by the effect of landscape composition on the aphid community. Further, our work has shown that intra-annual (within a growing season) variation and landscape composition interactively affect aphid community structure, and that aphid community composition has a significant effect on PVY prevalence.
There are economic and environmental imperatives for the development of biological disease control strategies for Potato Virus Y (PVY). PVY is an economically important crop disease that reduces yield and, in the worst cases, causes crop failure in many solanaceous crops, including potatoes, tomatoes, tobacco, peppers, and eggplants. PVY presents a daunting management challenge, because it is transmitted rapidly by a vast array of aphid species and infected plants can be difficult to identify in the field. Current strategies, such as pesticide applications and removal of infected plants from the field, are ineffective, needlessly increasing chemical inputs at both an economic and environmental cost.
1) Survey the main aphid vector species, common natural enemies of aphids, and the distribution and spread of PVY on small farms across several counties in New York State: I conducted this survey for two field seasons (2012 and 2013) and have completed this aspect of the project. The results of this work have been presented to growers in fact sheets, and will be published as two scientific papers.
2) Evaluate the influence of landscape-level effects: I have completed this part of the project. Using GIS software, I analyzed the landscape composition of the area surrounding the potato fields surveyed in Objective 1 at three scales: within radiuses of 0.5km, 1km, 1.5km. Land use was quantified as %agricultural, %forested, %developed, etc. There was a significant positive relationship between final virus prevalence and amount of agricultural land within all three scales in both years. Because the percent natural habitat was significantly negatively correlated with percent agriculture, it had the opposite relationship with final PVY prevalence. Percent agriculture also had a significant negative effect on aphid species richness in both years; the more agriculture was in the area, the fewer aphid species were present. Further analysis has demonstrated that percent agriculture interactively affects aphid abundance, species richness and functional community composition (here, the proportion of aphids that are PVY vectors) with intra-annual (within a growing season) variation.
3) Evaluate the influence of aphid community composition on PVY prevalence and spread: I have completed this part of the project. In field and greenhouse experiments conducted in the summer and fall of 2014, I examined the impact of aphid density and species diversity on aphid movement and PVY prevalence. Results indicate that the movement of a colonizing aphid species (one that settles and reproduces on potatoes) is more affected by the abundance of their conspecifics than the abundance of other species, and that different non-colonizing species affect their movement differently. Importantly, this project also demonstrates that aphid community composition (not movement or average transmission efficiency) has a significant effect on virus spread.
4) Evaluate the effect of natural enemy community composition on PVY prevalence and spread: Field populations of aphid natural enemies have very low abundances, did not have an effect on the aphid community in the landscape level project, and do not appear to be the main driver of PVY spread in this system. Because of this, I adjusted my original proposal to focus on the effect of the aphid vector community.
5) Disseminating disease control management strategies: Cumulatively, the data from the landscape project suggests that more natural habitat and less agricultural land surrounding an infected farm within a 1.5km radius will help minimize end-of-season PVY prevalence. These results emphasize the importance of prevention; purchasing disease-free seed tubers and not saving seed remain the best means of avoiding a PVY outbreak. This information, as well as data for each individual farm, was presented in fact sheets that were distributed to each participating grower.
Objective 1: Field survey of insect community composition and PVY prevalence.
I collected PVY prevalence and insect community data at more than 20 farms across several counties in New York State in a landscape level observational study. The sites were divided into two sampling groups: those sampled weekly, and those sampled 2-3 times during the season. At each site, I repeatedly sampled 20 randomly selected field plants to quantify PVY prevalence, and sampled the aphid and aphid predator communities using green tile water traps. Traps were collected after one week, and specimen were identified to species using morphological characters. At weekly sampled sites, I also monitored PVY prevalence using 20 potted Yukon Gold sentinel plants that were buried sporadically throughout the field. The infection status of plants was assessed using ELISA (enzyme-linked immunosorbent assay).
Objective 2: Landscape effects on insect community composition and PVY prevalence.
Using ArcGIS software and the USDA Crop Data Layer, I determine the percent area covered by crops, natural habitat, and developed land at a 0.5km, 1km, and 1.5km radiuses around the site. This data was analyzed in multivariate models with the data collected from Objective 1, to determine the relationship between landscape composition, insect community composition, and PVY prevalence.
Objective 3: Effect of aphid vector community composition on virus spread
In 2014, I conducted a mesocosm and a greenhouse study assessing the relationship between aphid density and community composition on aphid movement and PVY spread. I included three common aphid species found in Objective 1 in these studies, two low-transmitting (with PVY transmission efficiencies <0.1) non-colonizing (will not settle and reproduce on potato), Rhopalosiphon padi and Acrytosiphon pisum, and one high-transmitting colonizing species, Macrosiphum euphorbiae. In both experiments, the experimental unit was an array of 6 potato plants, arranged in a single row. In the mesocosm experiment, the plants were transplanted 10.2cm apart within 1m3 fine mesh cages in a field. The cages were arranged in 10 spatially separate blocks within the field. The experiment was replicated twice, with each replicate including 5 randomized blocks.
In a typical field situation, we would expect that colonizing aphids would generally be resident on plants throughout the season, whereas non-colonizers would visit briefly, and then depart. Hence, in the mixture and monospecific M. euphorbiae treatments, 30 wingless adult M. euphorbiae were placed on the first plant in the row, which was then bagged with a fine mesh fabric, and allowed to settle for 24 hours. In the monospecific A. pisum and R. padi low-density control treatments without M. euphorbiae (AP and RP), the first plant was bagged for the 24-hour settling period without aphids on it. After 24 hours, the mesh was removed and a second group of 30 wingless adult aphids was placed on the first plant, except in the M. euphorbiae low-density control treatment (ME), which had no second group of aphids. All plants were censused for aphids at four time points: 1, 3, 5, and 24 hours after the release of the second group of aphids. Aphid movement was quantified using two metrics: the proportion of aphids moving and plant occupancy (the number of aphids on recipient plants), which measures aphid-plant contact rate. The proportion of aphids moving is a relative measure of aphid movement, assessing the number of aphids that had moved to recipient plants (plant occupancy) as a proportion of the total number of aphids found in the array.
In the greenhouse experiment, the experimental procedure was similar to that described above, but the experimental set-up was slightly different. Plants were kept in pots and placed 15.2cm apart in a single row within black plastic flats. The PVY source plants were placed first in the row, and plants were arranged so that the leaves were touching The pots were filled to the brim with soil, causing the soil to overflow into adjacent pots, allowing for aphid movement between plants on the soil as well as direct movement from plant to plant. The experimental units were arranged in two blocks, one on either side of the greenhouse, and strips of cardboard painted with Tanglefoot (Contech, Goddard, KS 67052) separated each unit from those next to it, to prevent aphids from walking between arrays. After the completion of the bioassay, the PVY source plants were removed and composted and the recipient (initially uninfected) plants were sprayed with insecticide to kill all remaining aphids (Endeavor (EPA Reg.#100-913) and Avid (EPA Reg.#100-896)). The recipient plants continued to grow in the greenhouse for 4 weeks to allow the virus to replicate to detectable levels, at which time their foliage was sampled and frozen for later ELISA analysis.
During the summer of 2015, we carried out a field experiment designed to: 1) explore vegetation management strategies for PVY control; and 2) to further unravel the role of particular aphid species in PVY spread. Our experimental design included three treatments (monoculture potato, potato/oat polyculture, and potatoes with an oat border) factorially crossed with three levels of initial inoculum (0%, 5%, and 10% infected plants). We sampled plants for virus infection three times over the season and tracked aphid abundance and species richness using water traps. Data analysis suggested that oat borders had some potential to reduce the prevalence of PVY in comparison to potato monocultures, particularly at higher levels of initial infection, but this trend was not significant. Aphid numbers were low overall, and differences between treatments were not significant. The most common aphid early in the season was the colonizer M. euphorbiae. Later in the season, samples were dominated by noncolonizing aphids, with Uroleucon ambrosia occurring most often, followed by grain aphids (R. padi, R. maidis, and Sitobion avenae).
Objective 4: Effect of aphid natural enemy community composition on virus spread
In the analysis conducted in Objective 2, it became evident that aphid natural enemies had very low abundances throughout the study region. It also became clear that while the ladybug community significantly affected PVY prevalence, the effect of landscape composition on PVY prevalence was most likely mediated by the aphid community.
During the course of this project, I had 4 major findings:
- Landscape composition has a significant effect on final PVY prevalence on small, diversified farms in NY State. More specifically, sites with greater amounts of agriculture within 1500m of the site had greater PVY prevalence at the end of the growing season.
- The effect of landscape composition on final PVY prevalence is most likely mediated by the effect of landscape composition on the aphid community. Landscape did not have a significant relationship with the aphid predator (i.e. ladybug) community, but it did significantly affect the aphid community, and the aphid community significantly affected final PVY prevalence. The ladybug community also did not significantly affect the aphid community.
- Landscape composition interactively affects aphid abundance, species richness, and functional community composition (the proportion of aphids that were PVY vectors) with intra-annual (within season) variation. This supports the idea that the relationship between landscape composition and the aphid community will vary over time.
- Aphid community composition has a significant effect on PVY spread. This effect was not reflective of average transmission efficiency or species richness, but species identity.
My project has proceeded largely as expected with one major exception. While the ladybug community did have a significant effect on final PVY prevalence, it had no effect on the aphid community and was not affected by landscape composition, making it an unlikely mechanism for the effects seen in Objective 2. This caused me to shift the focus of the project onto the aphid community, specifically aphid community composition.
The data I have collected has provided useful information about the most common PVY aphid vectors and aphid natural enemy species, as well as the prevalence of PVY on small-scale farms across the Finger Lakes region. It has also demonstrated the impact of landscape composition on disease spread. This will allow for more effective estimation of the risk of in-season disease spread. My work has also shown that disease vector community composition, and specifically non-colonizing species, can play a significant role in PVY spread, indicating that further work should be done in these areas.
In addition, I have learned a great deal over the course of the last three years. I have gained project management and mentorship experience and learned several new research techniques, which will be essential as I progress in my career.
Education & Outreach Activities and Participation Summary
Throughout this project, I have participated in outreach both within and outside the scientific community. I have presented the results of this research at scientific conferences, produced one publication, and prepared three other manuscripts for publication, successfully finishing a doctoral thesis in the process. I have also compiled the results as fact sheets for participating growers, and created a blog directed at the general public that aims to raise awareness about public health issues (www.DirectTransmission.org), which was inspired by work on this project. The results of this project have also resulted in the development of a USDA-NIFA project investigating PVY across multiple scales, from viral genetic variation to landscapes.
The publications from this project include:
- Claflin, S.B., A.G. Power, and J.S. Thaler. 2015. Predators, host abundance, and host spatial distribution affect the movement of wingless non-colonizing vector Rhopalosiphum padi (L.) and PVY prevalence in an oat/potato system. Arthropod-Plant Interactions. doi: 10.1007/s11829-015-9370-3
- Claflin, S.B., L.E. Jones, J.S. Thaler, and A.G. Power. Simple landscapes have higher vector-borne plant virus prevalence. In review*.
- Claflin, S.B., N. Hernandez, R. Groves, J.S. Thaler, and A.G. Power. Intra-annual variation and landscape composition interactively affect aphid abundance, species richness, and functional community composition in two agricultural regions. In prep*.
- Claflin, S.B., A.G. Power, and J.S. Thaler. Aphid density and community composition differentially affect aphid movement and plant virus transmission. In review*.
*Articles listed as in prep were included as chapters in my doctoral thesis, which was successfully defended in February 2016.
Working directly with growers, the largest impact of my project was raising awareness, particularly about issues surrounding using saved (not certified) potato seed tubers. One grower I worked with switched between the two years of the observational survey project, and went from a final PVY prevalence of around 50% to a final prevalence of 0%. I did not receive any criticism or feedback about my project from growers.
The results of my work could impact growers in the future by changing their land use decisions and by improving disease risk assessments.
Areas needing additional study
The results of this work have illustrated that further research should be conducted on the PVY transmission efficiencies of non-colonizing aphid species, and that the impact of aphid community composition on PVY spread should be further explored.