Materials and Methods From 1988 to 2000, with the exception of 1992, 33 field-years of data on aphids, predators and parasitoids were collected in irr

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1 Corn Leaf Aphid, Rhopalosiphum maidis,, as a Key to Greenbug, Schizaphis graminum, Biological Control in Grain Sorghum, Sorghum bicolor G. J. Michels Jr. 1 and J. H. Matis 2 1 Texas Agricultural Experiment Station, Amarillo, TX, USA 2 Texas A&M Department of Statistics, College Station, TX, USA

2 Materials and Methods From 1988 to 2000, with the exception of 1992, 33 field-years of data on aphids, predators and parasitoids were collected in irrigated and rainfed grain sorghum fields. A field year is defined as one field sampled throughout the growing season. At the USDA-ARS ARS Crop Production Research Laboratory at Bushland, Potter Co., TX, data were collected for 12 years in irrigated and four years in rain-fed grain sorghum fields. At the Texas Agricultural Experiment Station North Plains Research Field at Etter, Moore Co., TX, data were collected for seven years in irrigated i and six years in rainfed grain sorghum fields. Two additional fields were sampled in Oldham Co. (irrigated) and in Gray Co., TX, (rainfed) in 1994 and two fields were sampled in Parmer Co., TX, (one irrigated and one rainfed) in Standard agronomic practices for grain sorghum production were followed each year. Fifty consecutive plants down a field row from a random starting point were examined by hand. Predator and parasitoid numbers/plant were recorded on standardized data sheets.

3 Materials and Methods After completing predator and parasitoid sampling, 12 plants were randomly selected from within the 50-plant sample, cut off at the base, and all corn leaf aphids and greenbugs were counted. The process was repeated 12 times at each sampling date, giving a total t of 600 plants sampled for predators and parasitoids id and 144 plants sampled for aphids. Different numbers of plants were sampled for beneficial insects and aphids in order to: 1. Obtain accurate aphid counts, especially corn leaf aphids which are often found deep in the whorl, 2. Time and personnel considerations, 3. Removing 600 plant per week from a particular field during the season could have adverse effects on the distribution of aphid and beneficial insects. The same sampling routine was carried out each year. We began observing fields in early June and sampling started when corn leaf aphids first began to appear in the field and continued on a weekly basis until greenbug densities dropped to zero for two consecutive weeks. At times, heavy rains prevented sampling on a strict seven- day interval. However, samples were taken as closely as possible to the planned sampling date.

4 The sorghum ecosystem is a wonderful world unto itself. As complex as many large-scale l systems. A primary producer (sorghum) hosts at least two herbivores (corn leaf aphid and greenbug), which are attacked by a number of predators and two to three species of parasitoids. In addition to being a convenient plant to work with, sorghum is an important source of grain for animal feed, and may become a source for biofuel feedstock. It is important to understand the interrelationships in this system if wise pest management decision are to be made. We ll start by looking at the players.

5 Corn Leaf Aphid, Rhopalosiphum maidis, is found annually on grain sorghum. Because it feeds in the whorl and upper leaves, it draws nutrient from the sink of the plant and causes little economic damage.

6 The greenbug, Schizaphis graminum, on the other hand, colonizes the bottom of the plant, the source, and redirects photosynthates away from the head, thus depriving i the developing head of the necessary nutrients t for good yield.

7 Greenbug damage is beginning to appear as reddish spots under the small colony.

8 These colonies grow rapidly, joining other colonies and covering the leaf

9 Greenbug damage can become very severe as noted on the bottom leaves of this plant.

10 The Convergent Ladybeetle, Hippodamia convergens, is the dominant ladybeetle species in Texas High-Plains i sorghum

11 The Sinuate Ladybeetle, Hippodamia sinuata, is the second most common ladybeetle in our sorghum fields

12 Wax-encrusted Scymnus pullus loweii larvae feeding on corn leaf aphids are commonly seen, but their impact is poorly understood.

13 A new player? The first Harmonia axyridis were recorded in sorghum in What will their future impact be on greenbug biocontrol? Other coccinellids found occasionally in our sorghum fields include Adalia bipunctata, Coleomegilla maculata, H. parenthesis, and Olla v-nigrum.

14 Aphids parasitized by Lysiphlebus testaceipes. Other parasitoid species include Aphelinus varipes and Diaeretiella rapae. Parasitoids are an important part of grain sorghum ecology. However, for this work their impact is not included. All parasitoid species attack aphids late in the season. In most cases this is long after the aphids have reached their peak abundance. Only when chemical applications are mismanaged do parasitoids play a crucial role in biological control.

15 The Problem and A Graphical Look at the Field Observations

16 In the early 1980s, aphids in sorghum were controlled by aerial chemical applications. Timing was based on seeing slick leaves caused by corn leaf aphid honeydew. Not a very sophisticated strategy! This method of control often required multiple applications. Spraying for corn leaf aphids often disrupted or eliminated predators. Research by Kring et al. (1985) clearly indicated that predaceous coccinellids were key to greenbug biological control, and this research prompted us to examine the interactions among the aphids and predators. Examples of the findings for corn leaf aphid and greenbug g for our 23 field-years follow.

17 Bushland Irrigated Greenbugs Corn Leaf Aphids Average s per Plant Aphid /23/88 7/29/88 9/7/88 6/28/89 8/2/89 6/13/90 7/18/90 8/29/90 7/20/92 8/26/92 7/23/93 8/27/93 7/22/94 8/24/94 7/19/95 8/23/95 7/11/96 8/13/96 7/21/97 8/25/97 6/30/98 8/6/98 7/14/99 8/24/99 6/15/00 7/24/00 8/28/00

18 Bushland Rainfed Corn Leaf Aphids Greenbugs Average ds per Plant Aphid1100 7/21/97 8/25/97 6/30/98 8/6/98 7/14/99 8/24/99 6/15/00 7/27/

19 Etter Irrigated Corn Leaf Aphids Greenbugs Average s per Plant Aphid1100 7/26/94 8/29/94 6/30/95 8/ /1/95 9/ /8/95 7/25/96 7/10/97 8/28/97 7/14/98 9/ /1/98 6/16/99 7/28/99 7/ /6/00 8/15/

20 Etter Rainfed Corn Leaf Aphids Greenbugs Average ds per Plant Aphid1100 7/20/95 8/25/95 7/3/96 8/14/96 6/26/97 8/1/97 9/11/97 6/23/98 8/5/98 6/30/99 8/19/99 7/18/

21 Other Irrigated: Oldham Co. 1994, Parmer Co Pla1600 Averag ge Aphids per ant Corn Leaf Aphids Greenbugs 7/8 8/94 8/1 11/9 7/3 3/95 8/7 7/95 9/1 12/9

22 Other Rainfed: Gray Co. 1994, Parmer Co Pla1600 Averag ge Aphids per ant Corn Leaf Aphids Greenbugs 7/8 8/94 8/1 11/9 7/3 3/95 8/7 7/95 9/1 12/9

23 All Fields Peak green nbug density y/plant Days deviation from sorghum boot stage when corn leaf aphids average 100 per plant Graphing peak greenbug density per plant vs. the deviation in days from the sorghum boot stage when corn leaf aphids reach an average of 100/plant indicates that greenbugs never reached damaging numbers when corn leaf aphids reached this abundance before boot stage.

24 S. graminum peak, Day 229 First S. graminum, Day 215 Predator peak, Day 212 R. maidis = 100, Day 195 R. maidis peak, Day 202 First predator egg, Day 200 Seasonal Occurrence of Aphids and Predators in Irrigated Sorghum Fields (95% CI) Sorghum Boot, Day Day of the Year - Ημέρα του έτους The seasonal events in irrigated fields associated with sorghum, the aphids, and predaceous coccinellids point to corn leaf aphid as a critical factor. Note that greenbug abundance peaks significantly after the predator peak.

25 S. graminum peak, Day 232 Predator peak, Day 216 R. maidis peak, Day 214 First S. graminum, Day 210 First predator egg, Day 206 R. maidis = 100, Day 202 Seasonal Occurrence of Aphids and Predators in Rainfed Sorghum Fields (95% CI) Sorghum Boot, Day Day of the Year - Ημέρα του έτους The seasonal events in rain-fed fields are much more variable, probably due to climatic conditions. The greenbug peak can occur within the predator peak. However, note that the first predator eggs are highly associated with corn leaf aphids, as in irrigated fields.

26 Coccinellid Adults and Larvae Coccinellid Egg Masses 1.25 nellids Cocci / 6/ 6/ 7/ 7/ 7/ 8/ 8/ 8/ 8/ 9/ 9/ 9/ 6/1 6/8 /15 /22 /29 7/6 /13 /20 /27 8/3 /10 /17 /24 /31 9/7 /14 /21 /28 The typical predator adult and egg mass abundance profile in grain sorghum, average of irrigated and rain- fed fields,

27 Corn Leaf Aphid Coccinellid Adults and Larvae Coccinellid Egg Masses Aph hids Coccin nellids / 6/ 6/ 7/ 7/ 7/ 8/ 8/ 8/ 8/ 9/ 9/ 9/ 6/1 6/8 /15 /22 /29 7/6 /13 /20 /27 8/3 /10 /17 /24 /31 9/7 /14 /21 /28 The Overlay typical of corn predator leaf aphid adult abundance and egg mass for the abundance same fields profile and years. in grain These sorghum, prey seem average to explain of irrigated the first predator and rain-fed peak, but fields, not the second.

28 Greenbug Coccinellid Adults and Larvae Coccinellid Egg Masses Aph hids Coccin nellids / 6/ 6/ 7/ 7/ 7/ 8/ 8/ 8/ 8/ 9/ 9/ 9/ 6/1 6/8 /15 /22 /29 7/6 /13 /20 /27 8/3 /10 /17 /24 /31 9/7 /14 /21 /28 Overlay of greenbug abundance for the same fields and years. These prey seem to explain the second predator peak, but not the first.

29 Corn Leaf Aphid Greenbug Coccinellid Adults and Larvae Coccinellid Egg Masses Aph hids Coccin nellids / 6/ 6/ 7/ 7/ 7/ 8/ 8/ 8/ 8/ 9/ 9/ 9/ 6/1 6/8 /15 /22 /29 7/6 /13 /20 /27 8/3 /10 /17 /24 /31 9/7 /14 /21 /28 Combination of both prey species seems to explain the two predator peaks observed in the field. How do the two prey species appear to the predators?

30 Combined Aphids Coccinellid Adults and Larvae Coccinellid Egg Masses Aph hids Coccin nellids / 6/ 6/ 7/ 7/ 7/ 8/ 8/ 8/ 8/ 9/ 9/ 9/ 6/1 6/8 /15 /22 /29 7/6 /13 /20 /27 8/3 /10 /17 /24 /31 9/7 /14 /21 /28 If corn leaf aphid and greenbug are looked at as a continuum of prey rather than distinct occurrences, the predator profile makes more sense.

31 Analyses Looking at predictive statistics for these data, correlations and simple linear regression analyses have yielded some very interesting results. The relationship of aphid peak abundance to the first observed coccinellid egg masses and predator peak abundance will be addressed first. Then a table and two graphs will illustrate how greenbug, corn leaf aphid and irrigation regime influence the peak coccinellid abundance in grain sorghum. The regressions are based on regressing the peak coccinellid abundance at sampling time t on aphid abundance at sampling time t-2.. This look back approach was employed using various steps back, with t-2 being found to be the most relevant. Prior to t-2, the predictions were too weak, and at t-1 and t the predictions hold little practical value. This makes sense, in that predator abundance tends to follow prey abundance, and there should be some optimal look back time that provides the best fit of the data. We hope to expand on these analyses in the future to provide more robust models. We believe that t these are key components to understanding di the system and open additional avenues for future research.

32 Correlation Coefficients for Aphids, Coccinellids, and Coccinellid Eggs R. maidis peak Predator peak Rainfed First egg Predator peak Irrigated First egg peak Prob S. graminum peak Prob R. maidis = Prob Corn leaf aphid and greenbug peak abundance were significantly correlated to predator peak abundance in irrigated sorghum, but not rainfed fields. Corn leaf aphid peak abundance was also significantly correlated to first egg in irrigated fields. However, these numbers can only be determined after the fact. The date when corn leaf aphid density nears 100/plant was significantly correlated to first egg and predator peak in both irrigated and rainfed fields, and is a number attainable in real time.

33 Simple Linear Regressions of Aphid Variables on Coccinellid Peak Abundance Equation R 2 p Interpretation All fields considered, irrigation regime not separated out C= SG ~ 30 SG for 1 ladybeetle C= A ~ 30 aphids for 1 ladybeetle C= SG+0.037RM ~ 37 RM or 34 SG for 1 ladybeetle C= I+0.037A Effect of RM>=100 by boot stage Paired field analyses, (1 irrigated, 1 rain-fed field), 10 comparisons, 20 fields C= SG ~ 24 SG for 1 ladybeetle C= A ~ 25 aphids for 1 ladybeetle C=6-(5*I)+0.025A ~ 25 aphids for 1 ladybeetle A = Any aphid, C = Coccinellid peak abundance, I= Indicator variable. For RM>=100, If RM>= 100, I=1,otherwise 0; for Paired field analyses, I=1 for irrigated, 0 for rainfed fields RM = R. maidis, SG= S. graminum

34 35 Peak Co occinellids/15 m of row Greenbugs alone All fields R 2 =0.77, p =0.024 Any aphid All fields R 2 =0.77, p = Aphids/plant If the fields are paired together across years and irrigation regimes (irrigated or rainfed), the peak coccinellid abundance is significantly related to both greenbug or total aphid abundance. The main difference is that when greenbugs alone are considered, the initial coccinellid abundance (y-intercept) is larger than when the aphid species is not considered. Therefore, corn leaf aphids and greenbugs are taken together as a food source probably better reflects the coccinellid peak that will be generated by a certain level of aphids in the field.

35 35 Peak Coccinellids/1 5 m of row Peak Coccinellids = 6 - (5*I) aphids R 2 =0.78, p = Irrigated Fields Rainfed Fields Aphids/plant Although we believe the corn leaf aphid trigger to be a crucial requirement for successful greenbug biological control, there are many other factors that come into play. For example, when irrigation is added as an indicator variable (1 if irrigated and 0 if rainfed) these two regressions indicate that irrigated fields have a higher initial coccinellid complement (y-intercept) than rainfed fields. This might be due to more rapid plant growth and earlier whorl formation in which corn leaf aphids prefer to feed, or just because the plants are generally larger and healthier which could influence coccinellid searching habits.

36 Results and Conclusions In irrigated sorghum fields,, the occurrence of the first predator eggs and peak predator abundance were significantly correlated to corn leaf aphid peak abundance and the date when corn leaf aphid abundance approaches 100/plant. Peak predator abundance in irrigated fields was also significantly correlated to greenbug peak abundance, but not to the occurrence of the first predator eggs. This result may be the critical factor or trigger of biological control of greenbugs because the appearance of corn leaf aphids early in the season probably initiates coccinellid oviposition, thus ensuring a captive population of larvae that are present to feed on greenbugs as they colonize the field. Failure of corn leaf aphids to colonize a field, or approach an abundance of 100/plant by the boot stage of sorghum probably bl results in few coccinellids ovipositing, and greenbugs not being subjected to predation sufficient to keep their numbers below economically damaging levels.

37 Results and Conclusions In rainfed sorghum fields,, the only significant correlation to the first occurrence of coccinellid eggs or peak predator abundance was the time when corn leaf aphid abundance approaches 100/plant. Corn leaf aphid and greenbug peak abundance were not significantly correlated. For greenbug management in either irrigated or rainfed grain sorghum, a seemingly handy rule of thumb is that greenbug biological control by coccinellids is successful and outbreaks do not occur when corn leaf aphids reach or exceed 100/plant by the time sorghum reaches the boot stage.

38 Results and Conclusions Regression analyses indicate that peak coccinellid abundance may be predicted by greenbug abundance or a combination of greenbug and corn leaf abundance, looking back to the aphid abundance two weeks prior to the coccinellid peak. The regressions are significant and have a high coefficient of determination (R 2 ). The regressions indicate that when corn leaf aphids and greenbugs are considered together as a common food source, a better indication of the initial coccinellid compliment is achieved than when greenbugs are considered alone. The greenbug only regression hints at a higher coccinellid abundance being present in the field when the greenbugs first enter the field, which could be due to the presence of corn leaf aphids. Although these regressions might not be a practical tool for assessing potential greenbug biological control, it does point to the need for further research and analyses of how far back can we look at aphid abundance and predict the coccinellid peak.

39 Results and Conclusions Both correlation and regression analyses indicate that it is probably better for research projectsto separate rainfed and irrigated fields, or at least pair a rainfed and irrigated field in the same location within the same year. In rainfed fields, regression analyses point toward a smaller compliment of initial coccinellids being present than in irrigated fields. This could be due to slower plant development and corn leaf aphid colonization causing coccinellids not to oviposit as readily as in irrigated fields. Finally, even with 33 field years of data, and 10 years of side-by side comparisons of irrigated and rainfed grain sorghum fields, there are still questions that need to be answered. The results point to a need to thoroughly assess climatic conditions, and perhaps look at the role non-coccinellid predators might play in the system. Although we did not add such predators as lacewings and syrphid fly larvae to our analyses, there is a chance that these minor predators play a role in specific years. All in all, the grain sorghum/aphid/predator hid/ d ecosystem remains an interesting ti and mysterious place that has been a joy to work in over the years.

40 Pertinent Historical Literature Kring, T. J., and F. E. Gilstrap Within field distribution of greenbug (Homoptera: Aphididae) and its parasitoids in Texas winter wheat. J. Econ. Entomol. 76: Kring, T. J. and F. E. Gilstrap Efficacy of three natural enemies of grain sorghum aphids (Homoptera: Aphididae). J. Kan. Entomol. Soc. 57: Kring, T. J., F. E. Gilstrap, and G. J. Michels, Jr Role of indigenous coccinellids in regulating greenbugs (Homoptera: Aphididae) on Texas grain sorghum. J. Econ. Entomol. 78: Kring, T. J. and F. E. Gilstrap Beneficial role of corn leaf aphid, Rhopalosiphum maidis (Fitch) (Homoptera: Aphididae) in maintaining Hippodamia spp. (Coleoptera: Coccinellidae) in grain sorghum. Crop Protection. 5: Rice, M. E. and G. E. Wilde Experimental evaluation of predators and parasitoids in suppressing greenbugs g (Homoptera: Aphididae) in sorghum and wheat. Environ. Entomol. 17:

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