Progress report for GS19-197

Project Type: Graduate Student
Funds awarded in 2019: $14,740.00
Projected End Date: 08/31/2021
Grant Recipient: University of Georgia
Region: Southern
State: Georgia
Graduate Student:
Major Professor:
Dr. Jason Schmidt
University of Georgia
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Project Information

Summary:

Pecan ranks in the top 10 commodities in Georgia with a farm gate value of $401 million in 2017. Like most agricultural production, pecans are threatened by attacks from insect pests. One key pest that concerns pecan growers and often times requires control are aphids, particularly, yellow aphids and black pecan aphids. Yellow pecan aphids can produce a considerable amount of honeydew, which promote sooty mold growth on foliage, negatively affecting the photosynthetic activity of the leaves. Black aphid feeding causes leaf chlorosis and, under heavy infestation, leaf defoliation. Growers normally respond to aphid pressure by spraying synthetic insecticides, which can negatively affect natural enemy populations and increases the risk of developing insecticide resistance, while only temporarily relieving the problem.

Therefore, there is a need for ecologically based methods of managing aphid populations such as biological control using parasitic wasps. Parasitic wasps are known to attack pecan aphids in Georgia but research is needed to investigate the relationships between yellow and black pecan aphids and their parasitoids.

Our objectives include: 1. identifying the parasitoid species attacking pecan aphids in Georgia and quantifying their parasitism rates; 2. assessing parasitism rates on pecan aphids in the laboratory; and 3. examining the relationship between canopy height and parasitism rates. We will sample aphids and collect parasitized aphids to quantify parasitism rates. We will deploy yellow sticky cards to survey for adult parasitoid populations. Adult parasitoids will be identified accordingly. Results will provide better understanding on how parasitoids contribute to aphid regulation and inform management decisions.

Project Objectives:

Our objectives include:

1. Identifying the parasitoid species attacking pecan aphids in Georgia and quantifying their parasitism rates. We have updated this objective to include a seasonal phenology of all threes aphid species and A. perpallidus (the primary aphid parasitoid in Georgia).

2. Assessing parasitism rates on pecan aphids in the laboratory (Canceled)

3. Examining the relationship between canopy height and parasitism rates. We also included the effects of canopy height on aphid and parasitoid numbers.

Cooperators

Click linked name(s) to expand
  • Dr. Ted Cottrell (Researcher)
  • Dr. Will Hudson (Educator and Researcher)
  • Dr. Jason Schmidt (Educator and Researcher)

Research

Materials and methods:

Objective 1: Examine parasitoid species attacking pecan aphids in major pecan-growing regions of Georgia

Objective 1. GPS coordinates, tree age and spacing, climate data, and the corresponding sampling periods for each site sampled. The Ray City site was only sampled in 2020.

All sampling sites were commercial orchards in major pecan growing regions in Central and South Georgia, USA. Site locations, sampling period, climate data, and site characteristics are listed in the table inserted above. During the 2019 and 2020 growing season, two 0.4 ha sampling areas (20.1 x 201.2 m each) were measured at each location prior to sampling. Within each sampling area, five mature ‘Sumner’ variety pecan trees were selected at random. From each tree, five leaves were collected from the lower canopy (~1-2 m from the ground) using a pole pruner and stored in labeled 3.79 L Ziploc® bags. Sampling was done every other week throughout the sampling period and sampling was ceased once growers began to harvest pecans. To standardize the leaf samples, only the middle three pairs of leaflets from each leaf were examined. Leaves were taken back to lab to quantify the number of live aphids and parasitized aphids (hereafter referred to as mummies; both hatched and unhatched). In 2020, unhatched mummies were placed individually in plastic capsules (Size 0, 7.62 cm, Healthy Life Supply; Mound House, NV) and stored in an environmental chamber (25°C, 60% RH, 16:8 L: D, Percival© E36L2; Perry, IA). Parasitoids that emerged from the mummies were identified as either primary or hyperparasitoids. This information was used to quantify the proportion of primary and hyperparasitoid emergence at each site. In addition to leaf sampling, one yellow sticky card (7.6 x 12.7cm, Olson Products Inc.; Medina, OH) was placed in the lower canopy of five randomly selected trees in each block (10 cards total) once a month from July to September in 2019 and from May to October in 2020 to assess adult A. perpallidus populations.

For all analyses, yellow and blackmargined aphids of all life stages (except eggs) were pooled together as the yellow aphid complex. All life stages of black aphid (except eggs) were pooled together. Mummy analysis consisted of both hatched and unhatched casings. Differences in seasonal mean aphid, mummy, and parasitoid adult numbers across the sampling period for each site and between sites were analyzed with a One-way Analysis of Variance. Tukey’s HSD was used for post hoc analysis to separate means among sampling dates and between sites at α = 0.05. Spearman correlation was used to analyze the correlation between aphids and both mummies and adult parasitoids at α = 0.05. All analyses were conducted in JMP® Pro 14.1.0 (SAS Version 14.1.0, Cary, NC).

Objective 2: Examining the parasitism rates of all three aphid species by pecan aphid parasitoids in the laboratory.

Canceled due to Covid-19 limiting lab experiments, have met with graduate committee in order to come up with and execute alternative projects.

Objective 3: Examining the relationships between canopy height and the rate of successful parasitism.

Objective 3. Layout of experimental design and collection dates for the elevation study.

This study was conducted from June – October 2020 in Peach County, Georgia, at the United States Department of Agriculture (USDA) Southeastern Fruit and Tree Nut Research Laboratory on mature ‘Stuart’ and ‘Sly’ pecan trees. All trees were ~15.2 meters or greater in height. A lift was used to perform all measuring and sampling. Prior to sampling, the tree canopies were measured and marked at 6 m, 9 m, 12 m, and 15 m in six trees in the orchard. To help increase aphid population in the experimental orchard, carbaryl + pyrethroid (Baythroid XL©, 119.8 g a.i./liter Bayer Cropscience) at 9.35 ml/ha was applied on 20 July and 3 August. Five compound leaves were taken from each height in each tree once a month to assess for aphid and mummy numbers. In addition, a yellow sticky card was placed at each height in each tree to quantify the adult parasitoid populations at each height.  

Leaves and cards were taken back to the laboratory to quantify the number of live aphids, mummies (both hatched and unhatched), and adult parasitoids. Since whole leaves were taken, the number of leaflets on each leaf was quantified. Effects of height on aphids and aphid parasitoids at the experimental orchard were analyzed with a One-way Analysis of Variance. Tukey’s HSD was used for post hoc analysis to separate means among sampling height at α = 0.05. Data were transformed using Square Root. Spearman’s correlation was used to analyze the correlation between aphids, mummies and adult parasitoid populations at α = 0.05. All analyses were conducted in JMP® Pro 14.1.0 (SAS Version 14.1.0, Cary, NC).

 

 

Research results and discussion:

Objective 1: Examine parasitoid species attacking pecan aphids in major pecan-growing regions of Georgia

Comparison across sampling locations

Figure 1. Comparison of yellow aphid complex, black aphids, and parasitoid pupa and adults between collection sites in 2019 and 2020. Different letters above each bar signify a significant difference using Tukey’s HSD at α = 0.05.

Mean densities of yellow aphid complex, black aphids, and mummies varied significantly across sites during the two years of sampling. Marshallville had significantly more yellow aphid complex than Albany or Nashville in 2019 (F= 12.02, DF = 2, 367 P<.0001; Fig. 1). In 2020, significantly more yellow aphid complex were found in Albany than in Nashville or Ray City (F= 7.451, DF = 3, 456 P<.0001; Fig. 1). Albany had significantly greater numbers of black aphids in 2019 compared to Marshallville or Nashville (F= 5.98, DF = 2, 367, P = 0.0028; Fig. 1). In 2020, black aphid numbers were significantly greater in Marshallville than in the other sites (F= 10.07, DF= 3, 456 P<.0001; Fig. 1). Mummy numbers were significantly greater in Marshallville than the other sampling sites in both 2019 and 2020 (F= 89.54, DF= 2, 367, P<.0001; F= 85.09, DF= 3, 456 P<.0001; Fig. 1). Marshallville also had a significantly greater number of adult parasitoids in 2019 among all the sites sampled (F= 5.5, DF= 2, 87, P= 0.0056; Fig. 1). In 2020, Ray City had significantly more adult parasitoids than Albany or Nashville (F= 4.33, DF = 3, 225 P= 0.0055; Fig. 1).

Figure 2. Proportion of primary and hyper parasitoids that emerged from unhatched mummies collected and reared from leaf samples in 2020. The proportions of parasitized aphids that did not emerge are also reported.

Proportions of primary and hyperparasitoids that emerged from mummies collected and reared in 2020 are shown in Figure 2. A majority (46% – 100%) of the unhatched mummies did not hatch under lab conditions. Mummified aphids collected from Marshallville, Albany, and Ray City had successful emergence of primary parasitoids, Aphelinus perpallidus, with 26%, 21%, and 46%, respectively. Hyperparasitoid emergence only occurred in pupa collected from Marshallville and Ray City with 16% and 8% respectively (Fig. 2). Preliminary morphological assessment has determined these parasitoids to be in the genus Syrphophagus (Hymenoptera:Encyrtidae). However, a molecular assessment will need to be performed to confirm specimen identity.  

Seasonal phenology of aphids and parasitoids at each location

Figure 3. Aphid and mummy numbers per leaf across the (A) 2019 and (B) 2020 sampling period and mean adult parasitoid numbers per card across the (C) 2019 and (D) 2020 sampling period at the Albany orchard. Different letters above each bar signify a significant difference using Tukey’s HSD at α = 0.05.

Albany. In 2019, the yellow aphid complex numbers varied significantly throughout the sampling period (F= 6.92, DF= 12, 117 P<.0001), peaking in mid-June before falling and rising slightly again in late July (Fig. 3A). Numbers remained until mid-October where it peaked again going into harvest season. Black pecan aphid numbers were also significantly affected by seasonality (F= 4.99, DF = 12, 117, P<.0001) with no captures until late September, increasing in mid-October and peaking in late October (Fig. 3A). Aphid mummy numbers varied significantly across the sampling period (F= 6.70, DF = 12, 117 P <.0001), remaining low throughout the season but experiencing a slight peak in October and November (Fig. 3A). Adult parasitoid numbers were not significantly affected by sampling time (F= 0.04, DF= 2, 27, P= 0.96; Fig. 3C).

In 2020, yellow aphid complex numbers again differed significantly across time (F= 7.36, DF= 11, 108, P<.0001), peaking in June before dropping significantly in July (Fig. 3B). Numbers increased slightly in early September but decreased again going into mid-October (Fig. 3B). Black aphid populations remained consistently low throughout the sampling period (F= 0.727, DF= 11, 108, P= 0.71; Fig. 3B). Aphid mummy numbers differed significantly across the season (F= 3.32, DF= 11, 108, P= 0.0006), with numbers in mid-October being significantly more than the peaks in May and late September (Fig. 3B). Adult parasitoid numbers were significantly greater in October, compared to the populations in August and May (F= 2.77, DF= 5, 53, P= 0.0269; Fig. 3D).

Figure 4. Marshallville aphid and mummy numbers per leaf across the (A) 2019 and (B) 2020 sampling period and mean adult parasitoid numbers per card across the (C) 2019 and (D) 2020 sampling period. Different letters above each bar signify a significant difference using Tukey’s HSD at α = 0.05.

Marshallville. In 2019, yellow aphid complex numbers were affected by seasonality (F= 15.90, DF= 11, 108, P<.0001(Fig. 4A).). Yellow aphid complex numbers were significantly greater in early June than any other time of the growing season. Black aphid numbers remained consistently low and did not significantly differ throughout the sampling period (F= 1.37, DF = 11, 108, P= 0.1953; Fig. 4A). Aphid mummy numbers in mid-August were significantly greater than any other time of the season except for early September and October (F= 14.20, DF= 11, 108, P <.0001; Fig. 4A). Adult parasitoids had greater numbers in July compared to August or September (F= 7.04, DF= 2, 27, P= 0.004; Fig. 4C).   

In the 2020 field season, yellow aphid complex numbers were significantly higher in late June than at any other point in the season (F= 6.90, DF= 11, 108, P<.0001; Fig. 4B). Black aphid numbers were significantly greater in late September than any other time in the sampling period except mid-October (F= 4.46, DF= 11, 108, P<.0001; Fig. 4B).  Numbers of aphid mummies began to rise in late June and continued to increase throughout the rest of the season peaking in September and October (F= 23.41, DF = 11, 108, P<.0001; Fig. 4B). Adult parasitoid numbers were significantly greater in September compared to May, June, August, and October. Numbers in May and June were significantly less than July (F= 6.03, DF= 5, 54, P= 0.0002; Fig. 4D).  

Figure 5. Nashville aphid and mummy numbers per leaf across the (A) 2019 and (B) 2020 sampling period and mean adult parasitoid numbers per card across the (C) 2019 and (D) 2020 sampling period. Different letters above each bar signify a significant difference using Tukey’s HSD at α = 0.05.

Nashville. In 2019, for the yellow aphid complex, late May had the greatest number of aphids compared to the rest of the growing season (F= 22.50, DF= 11, 108, P<.0001). The rest of the season had very low to no aphid numbers and there was no significant difference among the rest of the sampling dates (Fig. 5A). Black aphid numbers were low and did not significantly differ at any point in the sampling period (F= 1.80, DF= 11, 108, P= 0.06; Fig. 5A). Aphid mummy numbers did not significantly differ across the sampling period (F= 1.63, DF= 11, 108, P= 0.09; Fig. 5A). Adult parasitoid numbers were significantly greater in July compared to the August and September (F= 32.1, DF= 2, 27, P<.0001; Fig. 5C).

In 2020, yellow aphid complex numbers were significantly greater in late May compared to all other sampling periods with few or no aphids found (F= 9.58, DF= 11, 108, P<.0001; Fig. 5B). No significant difference was found in black aphid numbers during the sampling period (F= 1, DF= 11, 108, P= 0.4513; Fig. 5B), with no black aphids collected except in early August. Aphid mummies were significantly greatest in Mid-August but were overall low to absent throughout most of the sampling periods (F= 3.51, DF = 11, 108, P= 0.0003; Fig. 5B), with no significant difference among any of the other sampling periods. Adult parasitoid numbers were statistically equal throughout the sampling period (F= 2.07, DF= 5, 54, P= 0.082; Fig. 5D).  

Figure 6. Ray City aphid and mummy numbers per leaf across the 2020 sampling period (A) and adult parasitoid numbers per card across the 2020 sampling (B). Different letters above each bar signify a significant difference using Tukey’s HSD at α = 0.05.

Ray City. The Ray City orchard was only sampled in 2020. Yellow aphid complex numbers in Ray City were low throughout the growing season with early October having significantly higher numbers compared to the rest of the sampling period except early June and mid-October (F= 9.45, DF= 9, 90, P<.0001; Fig. 6A). Black aphid numbers did not significantly differ throughout the sampling period (F= 0.890, DF= 9, 90, P= 0.538; Fig. 6A), with populations occurring only in early June and late July. Aphid mummies were statistically similar throughout the year with the exception of mid-October where numbers were significantly greater than late June and mid-August (F= 2.13, DF= 9, 90 P= 0.035; Fig. 6A). Adult parasitoid numbers did not significantly differ across the sampling period (F= 1.21, DF= 4, 45, P= 0.321; Fig. 6B).

Relationship between aphid populations and parasitoids

At the Albany site in 2019, there was a positive correlation between aphid mummies and black aphids (Spearman ρ = 0.2653, P= 0.0023). In Marshallville, adult parasitoid populations were positively correlated with yellow aphid complex populations (Spearman ρ= 0.5126, P= 0.0038), while aphid mummies were negatively correlated with yellow aphid complex numbers (Spearman ρ= -0.4235, P<.0001).  In Nashville, aphid mummies and yellow aphid complex numbers were positively correlated (Spearman ρ= 0.406, P<.0001).

In 2020, there was a significant positive correlation between aphid mummies and black aphids in Marshallville (Spearman ρ= 0.4481, P<.0001). In Ray City, both adult parasitoids and aphid mummies were positively correlated with the yellow aphid complex (adult parasitoids and yellow aphids: Spearman ρ= 0.3011, P= 0.0336; mummies and yellow aphids: Spearman ρ= 0.2051, P= 0.0407).

Discussion

Comparison of aphids and parastioids at each site in both years revealed variation among sites across both years of the study with little consistency from year to year. The only consistent trend among the sites was that Marshallville had the highest number of parasitoids during both years of the study. One interesting aspect of this analysis is that it suggests that intensive spraying may not be necessary to achieve low aphid density. Based on the brief snapshot of overall aphid numbers provided, aphid number could be significantly different in an intensively spray orchard versus one that was not in one year and then be statistically similar in the other. Long term assessment over several growing seasons may be necessary to properly assess trends and patterns between these sites.

The proportion of primary parasitoids that emerged from the collected mummies was lower than those of a previous study done in Texas which reported A. perpallidus emergence of 48.3%, 60.3%, and 60.3% across three sites (Bueno Jr and Stone 1983). Hyperparasitoid emergence was much higher in our study at 8% and 16% compared to 1.2%, 1.7%, and 3.3% emergence rates in the Texas study. It should also be noted that the authors of the Texas study acquired many more mummies during their study (1328) than in this one (376). Collection method likely explains these differences where the Texas study collected aphids and observed them for mummification in the lab whereas the mummies in this study were collected directly from the field. This likely allowed for the authors to collect mummies that were fresher and less exposed to harsh environmental conditions resulting in higher primary emergence. This may also explain the lower hyperparasitism rates in their study as the aphid mummies collected may have not been in the field long enough to be attacked by hyperparasitoids. Aphid hyperparasitoids have been studied to prefer attacking aphid mummies than non-mummified parasitized aphids (Buitenhuis et al. 2004).

Regardless of site, yellow aphid numbers typically followed a similar pattern of rising and crashing throughout the season with peaks usually occurring in May and June followed by another peak in late September and early October. Black aphids were rarely collected throughout the growing season usually being found in low numbers in September and October. The population trends in our data are similar to previous studies on aphid phenology and life history (Tedders 1978, Dutcher et al. 2012). Interestingly, despite insecticide application at the sites in this study, aphid numbers still peaked at similar times as peaks at the unsprayed experimental orchards of other studies. However, the growth of these peaks does not appear to be as great. Aphids collected during this study seem to achieve their highest abundance between May and June and September and October. Interestingly, this lines up with the times in which growers have either not begun to treat for aphids or have ceased treating for aphids.

While it appears that aphid phenology has not shifted significantly compared to previous studies it does appear that aphid abundance has decreased, especially since the 1970’s. The late 1970’s study by W.L. Tedders in Byron, Georgia found an average number of 100 aphids per 25 leaves during seasonal peaks with blackmargined aphid averaging around 900 per 20 leaves around October and December (Tedders 1978). J. Dutcher’s 2006-2011 study found numbers closer to ours, but still found that during the peak aphid numbers could get as high as 40-100 aphids per shoot (Dutcher et al. 2012). This is much higher than our highest average peak of 10 aphids which was in May of 2019 in Marshallville, GA. While insecticide application pressure could be possible explanation for this, aphid numbers in our commercial orchards were low even before the first insecticide application of the season and during the months when growers had ceased management. Additional factors that explain this could range from changes in climate or simply a natural lull in aphid numbers as can be seen in Dutcher’s previous long-term study (Dutcher et al. 2012). Variety could also play a factor in why aphids were not found in great abundance. While Sumner is an aphid susceptible variety and was the sole variety examined at each site, Sumners shared orchard space with other varieties that could potentially be more susceptible. This could explain low numbers in Sumners at the Albany site despite a low-spray schedule as other aphid-susceptible varieties such as Gloria Grande were also present at the site. A previous studies showed that cultivar type can have a significant effect on aphid numbers, as was shown with Cheyenne pecans having a much greater aphid density than Kiowa or Pawnee planted in the same area (Honaker et al. 2013). A key difference between this study and Tedder’s study is the types of insecticides used then, which primarily consisted of broad-range insecticides such as organophosphates and pyrethroids (Holloway 1976, Harris and Cutler 1977), and today which consists primarily of insecticides that primarily target piercing, sucking insects (Mulder et al. 2018, Acebes-Doria and Halliday 2020). In addition, Harmonia axyridis (Coleoptera: Coccinellidae), the multicolored Asian lady beetle, has become established in Georgia since that time where it has become an effective biological control agent of pecan aphid (Mizell 2007).

The adult parasitoid phenology typically exhibited a similar trend to the aphids in terms of peaks and crashes. This suggests that adult parasitoid numbers rise and fall with that of their host. This can be supported by the positive correlation we found between adult parasitoids and aphids in Marshallville in 2019 and Ray City in 2020.  Aphid mummies were different in their correlation with aphid numbers. While we did find a positive correlation between mummies and yellow aphid numbers in a few sites, we found a strong negative correlation between yellow aphid numbers and mummies in Marshallville in 2019. This can possibly be explained by the persistence of mummies on the leaf when other factors, such as insecticide application, rainfall, or natural population crashes eliminate the aphids in an area. Even after the parasitoid has hatched, the remaining pupal case can be found on the leaf afterwards. This makes it difficult to draw a strong correlation between aphid and aphid mummy numbers as mummies can persist long after a population of aphids is gone. A previous study in far west Texas saw a similar trend when blackmargined aphids were sprayed (Bueno Jr and Stone 1985). They attributed this to having an ample number of aphids available to sustain A. perpallidus populations even after treatment. Several previous studies have assessed aphid mummies and parasitism rates in correlation with pecan aphids numbers, but assessment of adult numbers is lacking (Bueno Jr and Stone 1983, Bueno Jr and Stone 1985). Our study is one of the first studies to look at population density of adult A. perpallidus in the field.

The assessment of black and yellow pecan aphid populations throughout the year is important in establishing management programs for each species. In south Georgia, growers are typically not concerned with yellow aphids if they are present in low numbers. Personal communication with growers at Ray City and Marshallville revealed that little to no effort is currently put towards yellow aphid management due to current low population numbers. The growers in this study however expressed much greater concern for black pecan aphid which they felt were a bigger threat to trees as they can cause more damage at lower numbers. This reflects the standards specified in the University of Georgia pecan spray guide (Acebes-Doria and Hudson 2020) which discourages spraying of yellow aphid in the early season and only spraying when there are large amounts of honeydew present. Meanwhile, it is recommended to treat black aphids if as few as one black aphid is found after checking 10 terminals on 10 trees after the first of July (Acebes-Doria and Hudson 2020). 

Overall, this study was one of first to perform a multi-site assessment of pecan aphid and A. perpallidus populations in commercial pecan orchards. While the study did not find any significant changes in aphid phenology it did reveal potential decreases in aphid populations since the 1970’s. Additional years of study may be necessary to see if this is a long-term decrease or a temporary lull in populations. This study was also among the first to plot a seasonal phenology for adult A. perpallidus. Future studies could help expand upon this and help reveal long-term population trends. The literature available on this topic is currently quite limited and many of the points analyzed in this study could be further examined to reveal more information. Further regular and continued assessment is important to help growers develop pecan aphid management plans.

Literature Cited

  • Acebes-Doria, A. L., and W. G. Hudson. 2019. 2020 Commercial Pecan Spray Guide. Univ. Georgia Coop. Ext. Pub. 841.
  • Acebes-Doria, A. L., and P. L. Halliday. 2020. Insecticide Efficacy Against Pecan Aphids and Pecan Leaf Scorch Mites, 2018. Arthropod Manag. Tests. 45.
  • Bueno Jr, R., and J. Stone. 1983. Phenology of a parasite of the blackmargined aphid in west Texas [Aphelinus perpallidus, Monellia caryella]. Southwest. Entomol. 8: 73-79.
  • Bueno Jr, R., and J. D. Stone. 1985. Aphelinus Perpallidus Parasitism of Monellia Caryella Populations in Far West Texas. J. Entomol. Sci. 20: 325-330.
  • Buitenhuis, R., G. Boivin, L. Vet, and J. Brodeur. 2004. Preference and performance of the hyperparasitoid Syrphophagus aphidivorus (Hymenoptera: Encyrtidae): fitness consequences of selecting hosts in live aphids or aphid mummies. Ecol. Entomol. 29: 648-656.
  • Dutcher, J. D., H. Karar, and G. Abbas. 2012. Seasonal Abundance Of Aphids And Aphidophagous Insects In Pecan. Insects 3: 1257-1270.
  • Harris, M. K. and B. L. Cutler. Pecan, Black Pecan Aphid Management, 1977
  • Holloway, R. L. Yellow Pecan Aphid Control on Pecan, 1976. Insecticide and Acaricide Tests. 3.
  • Honaker, J., S. Skrivanek, J. Lopez, D. Martin, L. Lombardini, L. Grauke, and M. Harris. 2013. Blackmargined aphid (Monellia caryella (Fitch); Hemiptera: Aphididae) Honeydew Production in Pecan and Implications for Managing the Pecan Aphid Complex in Texas. Southwest. Entomol. 38: 19-32.
  • Mizell, R. F. 2007. Impact of Harmonia Axyridis (Coleoptera: Coccinellidae) on Native Arthropod Predators in Pecan and Crape Myrtle. Fla. Entomol. 90: 524-536.
  • Mulder, P. G., S. K. Seuhs, M. E. Payton. 2020. Insecticide Efficacy for Controlling Pecan Aphids, 2018. Arthropod Manag. Tests. 45.
  • Tedders, W. 1978. Important biological and morphological characteristics of the foliar-feeding aphids of pecan. USDA Technical Bulletin. 1579.

Objective 3: Examining the relationships between canopy height and the rate of successful parasitism.

In 2019, A. perpallidus adult numbers did not differ between heights in either the September or October collection dates (F= 0.28, DF= 3, 12, P= 0.8391 (Sept.)(F= 0.8556, DF = 3, 20, P= 0.4801). No leaf samples were collected in 2019 due to low aphid numbers.

Figure 7. Mean number of aphids, mummies, and adult A. perpallidus collected per leaf/card during each sampling date and throughout the whole season at the experimental orchard in 2020. Presence of differing letters designates a significant difference between the four canopy locations using Tukey’s HSD at α = 0.05.

Aphids and Mummies. In 2020, leaf samples revealed little effect of canopy height on pecan aphid numbers throughout the season. Yellow pecan aphids varied statistically by height only during the 8 August sampling, where aphid numbers at 6 m were statically greater than aphid numbers at 12 and 15 m  and 9 m aphid numbers were statistically greater than 15 m (F= 9.28, DF= 3,20, P= 0.0005; Fig. 7). Total seasonal numbers of yellow pecan aphids were statistically greater in 6 m than at 12 and 15 m and 9 m aphid numbers were statistically greater than 15 m (F= 7.5, DF= 3, 116, P= 0.0001; Fig. 7). Black aphid numbers differed only during the 14 October sampling, where there were statistically more black aphids at 6 m than at 15 m (F= 4.23, DF= 3, 20, P= 0.0181, Fig. 7). The numbers of mummified aphids were statistically different during the 16 June sampling when mummies were more abundant at 6 m than at 9 m or 15 m (F= 3.19, DF = 3, 20, P= 0.046, Fig. 7). 5 August sampling where mummies were statistically more abundant at 6 m than at 15 m (F= 3.42, DF= 3, 20, P= 0.0370, Fig. 7)  In addition, the season-long mummy numbers were higher at 6 m than at 15 m (F= 4.77, DF= 3,116, P= 0.0036; Fig. 7).

Aphelinus perpallidus. Adult A. perpallidus numbers in 2020 followed a similar trend to yellow pecan aphid. The only statistical difference in height was found during the 8 August sampling period where adult A. perpallidus numbers were statically greater at 6 and 9 m than at 12 and 15 m (F= 3.72, DF = 3, 20, P= 0.0283; Fig. 7). Analysis of season-long numbers revealed that adult A. perpallidus numbers were statically greater at 9 m in the canopy than at 12 or 15 m in the canopy (F= 4.87, DF = 3, 116, P= 0.0031; Fig. 7). There was no statistical difference in the other heights throughout the season.

Relationship between Aphids and Parasitoids According to Height. Spearman’s analyses suggest a relationship between yellow aphids, aphid mummies, and A. perpallidus. At 6 m, aphid mummy numbers and yellow aphid numbers were positively associated with each other (Spearman ρ= .6179, P= 0.0003). Aphelinus perpallidus numbers were positively correlated with both yellow aphid numbers (Spearman ρ= 0.596, P= 0.0005) and aphid mummy numbers (Spearman ρ= 0.4256, P= 0.019). At 9 m in the canopy, yellow aphid numbers were positively correlated with both aphid mummy numbers (Spearman ρ= 0.3852, P= 0.0356) and A. perpallidus numbers (Spearman ρ= 0.5923, P= 0.0006). At 12 m, the only positive correlation was found between A. perpallidus numbers and yellow aphid numbers (Spearman ρ= 0.3739, P= 0.0418). No correlations were found at 15 m in canopy height.

Discussion

This experiment suggests that populations of aphids and their parasitoids can possibly be affected by canopy height. However, this trend is more apparent when one views overall populations throughout the season rather than on a month to month basis. During this experiment we only saw a significant difference in height effects on yellow aphids and adult parasitoids in early August. This can possibly be attributed to July-August being a peak time of the year for yellow aphids and they may have spread more readily through the canopy due to a growing population (Wells and Conner, 2007). This would have also triggered a response from their parasitoids which would have followed them through the canopy. Analysis of the overall season revealed that aphids, mummies, and adult parasitoids are more abundant at the lower two heights, this may be a way to avoid environmental factors such as sunlight, heat, rain, and wind. Regardless, it is still impressive to see that both prey and parasitoid can still colonize trees up to 15.2 meters in height despite potentially dispersal limits due to size and mobility.  This can be useful as it means parasitoids can possibly be relied upon to manage pest populations in the upper canopy. This can be helpful as sprayers sometimes can struggle to apply the upper canopy. A study looking at spray coverage at different heights in mature pecan trees, has shown that spray coverage decreases significantly as canopy height increases (Bock et. al, 2015). This indicates that parasitoids can play a key role in pest management in areas where insecticidal control may fail.

The effects of elevation on natural enemies is poorly understood and analysis of a single family or even species should not be used as a blanket statement for all beneficial insects. A study on lady beetle (Coleoptera:Coccinellidae) populations at different heights revealed that lady beetles may respond negatively, neutrally, or positively to height depending on the species (Cottrell, 2017). A study on Ichneumonid wasps found that the community differed between the lower canopy and the upper canopy. Certain groups of Ichneumonid were captured in one location over the other while the other groups were captured equally in both locations (Di Giovanni et al. 2015). In addition, studies assessing parasitism rates of leaf-chewing pest found that parasitism rates increased from the first level (area closest to the ground floor) to the third level (uppermost area of a given tree) in smaller tree species and decreased from first level to the third level in taller tree species (Šigut et al. 2018). This phenomenon in smaller trees was believed to be due to spatial avoidance of predators by parasitoids. Since predators were more abundant in the first level, which was close to the forest floor, parasitoids may have moved higher in the tree to avoid predation. For the taller tree species, it was argued that parasitoids avoid the harsh abiotic conditions of the third level and thus are more prevalent in the lower, two levels. In addition, due to the first level being much farther from the forest floor there was less risk of predation (Šigut et al. 2018). This suggests that all natural enemies are not effected by elevation equally even on a species to species level. Future studies should look at the effects of elevation on numerous species of natural enemies in order to fully understand canopy height effects.    

Literature Cited

  • Bock, C. H., M. W. Hotchkiss, T. E. Cottrell, and B. W. Wood. 2015. The Effect of Sample Height on Spray Coverage in Mature Pecan Trees. Plant Dis. 99: 916-925.
  • Cottrell, T. 2017. Trap Height Affects Capture of Lady Beetles (Coleoptera: Coccinellidae) in Pecan Orchards. Environ. Entomol. 46: 343-352.
  • Di Giovanni, F., P. Cerretti, F. Mason, E. Minari, and L. Marini. 2015. Vertical stratification of ichneumonid wasp communities: the effects of forest structure and life‐history traits. Insect Science 22: 688-699.
  • Šigut, M., H. Šigutová, J. Šipoš, P. Pyszko, N. Kotásková, and P. Drozd. 2018. Vertical canopy gradient shaping the stratification of leaf‐chewer–parasitoid interactions in a temperate forest. Ecology and evolution 8: 7297-7311.
  • Wells, L., and P. Conner. 2007. Southeastern Pecan Growers’ Handbook.

 

 

Participation Summary
4 Farmers participating in research

Educational & Outreach Activities

1 Journal articles
1 Published press articles, newsletters
1 Webinars / talks / presentations

Participation Summary

Education/outreach description:

Due to the covid-19 pandemic, many conferences were canceled which limited the ability to perform outreach. However, we were able to do a couple things to fulfill this requirement. In 2020, at the virtual National Entomological Society of America (ESA) meeting, a virtual poster was presented that detailed the results collected during the 2020 field season for the elevation study (Objective 3). A poster will be presented at the 2021 Southeastern branch meeting that will detail the findings of the Seasonal Phenology study (Objective 1). In addition, we have submitted an article to The Pecan Grower magazine for publication in a future issue over the seasonal phenology (Objective 1) and have also submitted a research manuscript to the Journal of Environmental Entomology for the same objective that is currently in review.

Presentations

  • Entomological Society of America National Meeting. Effects of Vertical Stratification on the Abundance of Pecan Aphid Parasitoids in Georgia Pecan Orchards. Slusher, E.K., T. Cottrell, A.L. Acebes. November 11-25 2020, Virtual
  • Entomological Society of America Southeastern Branch Meeting. Multi-Site Seasonal Monitoring of Pecan Aphids and Their Parasitoids in Commercial Pecan Orchards. Slusher, E.K., W. Hudson, A.L. Acebes. March 29-31 2020, Virtual

Publications

  • The Pecan Grower Magazine (To be published). Multi-Site Seasonal Monitoring of Pecan Aphids and Their Parasitoids in Commercial Pecan Orchards. Slusher, E.K., W. Hudson, A.L. Acebes.
  • Journal of Environmental Entomology (In review). Multi-Site Seasonal Monitoring of Pecan Aphids and Their Parasitoids in Commercial Pecan Orchards. Slusher, E.K., W. Hudson, A.L. Acebes.

Project Outcomes

Project outcomes:

Based off the findings of objective 1, it has become apparent that pecan aphid numbers are much lower than what they were in the past. Two of the orchards we studied during this research applied few insecticides throughout the year while two orchards sprayed more frequently. Despite this, orchards that sprayed less frequently still had very low aphid numbers.  This may indicate that growers in Southeast Georgia may not need to apply insecticides at a high frequency in order to manage pecan aphids. This can have both economic and environmental benefits as growers may be able to mitigate insecticide application thus saving money while also reducing the amount of insecticide that makes its way into the surrounding environment. In objective 3, we found that parasitoids can still colonize the upper canopy of pecan trees. This indicates they may be able to provide some sort of control to aphids in the upper canopy. This can have economic and environmental benefits as well as growers can rely on natural enemies to provide biological control even in the upper canopy of pecan trees.

Knowledge Gained:

My advisor and I have gained a better understanding of the ecological relationships between pecan aphids and their parasitoids. Prior to the research done in objective 1, little research had been done on the seasonal phenology of pecan aphids and their parasitoids in commercial orchards in the Southeast. Prior studies done in the Southeast were primarily restricted to single experimental orchards. In addition, little to no analysis of the seasonal phenology of adult Aphelinus perpallidus  had been done prior to this study. We have also gained a better understanding of how populations of pecan aphid and A. perpallidus vary at different commercial sites and also how diverse grower management tactics are. Talking with growers has allowed us to understand their concerns with regards to pecan management which allows us to adjust future studies accordingly. For example, as previously mentioned, Georgia growers are often more concerned with black pecan aphid than yellow pecan aphid, and thus future studies can be crafted to help growers manage black pecan aphid more effectively. In objective 3, we have learned more about the effects of elevation on pecan aphids and their parasitoids. The effects of elevation on pests and natural enemies in pecan orchards has been a poorly studied topic and is important when addressing pecan pests. Knowing where in the tree that certain insects have a preference for can help spot discrepancies and overlap in pest and predator/parasitoid populations. 

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.