Corn Leaf , maidis, as a Key to Greenbug , graminum, Biological Control in Grain ,

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 Materials and Methods

• From 1988 to 2000, with the eexceptionxception of 1992, 33 “field-“field-years”years” of data on , predators and parasitoids were collected in irrigated and rainfed grain sorghum fields. • A “field year” is defined as one fifieldeld sampled throughout the growing season. • At the USDA-USDA-ARSARS Production Research Laboratory at BhldPttCTXdtBushland, Potter Co., TX, data were co lltdf12llected for 12 years in irrigated and four years in rain-rain-fedfed 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 iiirriga tdted an d s ix years in ra ifdinfed gra in sorg hum fildfields. • 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 irrig ated and one rainfed) in 1995. • 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. Materials and Methods • After completing predator and parasitoid sampling, 12 plants were randomly selected from within the 50-50-plantplant 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 tot al of 600 pl ant s sampl ed f or pred at ors and parasit o ids an d 144 plants sampled for aphids. • Different numbers of plants were sampled for beneficial 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. Remov ing 600 pl ant per week f rom a parti cu lar fie ld dur ing the season could have adverse effects on the distribution of aphid and beneficial insects. • The same samppgling routine was carried out each year. We be gan 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, heavyyp rains prevented sam pgpling on a strict seven-seven- day interval. However, samples were taken as closely as possible to the planned sampling date. The sorghum ecosystem is a wonderful world unto itself. As complllex as many largearge--scascallle systems. A primary producer (sorghum) hosts at least two herbivores ((pcorn 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 feed, and may become a source for biofuel feedstock.

It is important to understand the interrelationships in this system if wise management decision are to be made.

We’ll start by looking at the players. Corn Leaf Aphid, , 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. The greenbug, , on the other hand, colonizes the bottom of the plant, the source, and redirects photosynthates away from the head, thus depr iithdiving the deve liloping hdfthhead of the necessary nu titftrients for goo dildd yield. Greenbug damage is beginning to appear as reddish spotdthlllts under the small colony. These colonies grow rapidly, jjgoining other colonies and covering the leaf Greenbug damage can become very severe as noted on the bottom leaves of this plant. The Convergent Ladybeetle, Hippodamia convergens, is the dominant ladybeetle speciiTies in Texas HihHigh-Pla ins sorg hum The Sinuate Ladybeetle, Hippodamia sinuata, is the secondtd most common ladybeetle in our sorghum fields WaxWax--encrustedencrusted Scymnus pullus loweii larvae feeding on corn leaf aphids are commonlbtthiitilly seen, but their impact is poorly understood. Al?ThfitA new player? The first HiidiHarmonia axyridis were recorded in sorghum in 2007. What will their future impact be on greenbug biocontrol? Other coccinellids found occasionallyyg in our sorghum fields include Adalia bipunctata, Coleomegilla maculata, H. parenthesis, and Olla vv--nigrumnigrum. Aphids parasitized by . Other parasitoid species include Aphelinus varipes Parasitoids are an and . important part of grain sorghum ecology. However, for this work their ititimpact 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. The Problem and A Graphical Look at the Field Observations 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 ffffor 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 amonggp the aphids and predators. Exam ples of the findin gs for corn leaf a phid and greenbu g for our 23 “field“field--years”years” follow. Bushland Irrigated

2000 1900 1800 Greenbugs 1700 nt 1600 aa Corn Leaf Aphids 1500 1400 1300 1200 s per Pl s per 1100 1000 900 800

e Aphid 700 gg 600 500 400

Avera 300 200 100 0 1/97 5/97 0/98 4/99 4/99 5/00 4/00 8/00 3/88 9/88 8/89 3/90 8/90 9/90 0/92 6/92 3/93 7/93 2/94 4/94 9/95 3/95 1/96 3/96 /6/98 /7/88 /2/89 22 22 33 11 22 11 22 22 22 22 22 11 11 22 22 22 22 22 22 22 11 22 11 11 88 99 88 6/ 7/ 6/ 6/ 7/ 8/ 7/ 8/ 7/ 8/ 7/ 8/ 7/ 8/ 7/ 8/ 7/ 8/ 6/ 7/ 8/ 6/ 7/ 8/ Bushland Rainfed

2000 1900 1800 1700 nt 1600 aa Corn Leaf Aphids 1500 1400 Greenbugs 1300 1200 s per Pl s per 1100 dd 1000 900 800

e Aphi 700 gg 600 500 400

Avera 300 200 100 0 1/97 5/97 0/98 4/99 4/99 5/00 7/00 /6/98 22 22 33 11 22 11 22 88 7/ 8/ 6/ 7/ 8/ 6/ 7/ Etter Irrigated

2000 1900 1800 1700 Corn Leaf Aphids nt 1600 aa Greenbugs 1500 1400 1300 1200 s per Pl 1100 1000 900 800

e Aphid 700 gg 600 500 400

Avera 300 200 100 0 0/97 8/97 4/98 1/98 6/99 8/99 6/00 5/00 6/94 9/94 0/95 1/95 8/95 5/96 // // // // 11 22 11 11 22 11 22 22 33 22 9 7 8 9 7/ 8/ 6/ 7/ 7/ 8/ 7/ 6/ 7/ 8/ Etter Rainfed

2000 1900 1800 1700 nt 1600 Corn Leaf Aphids aa 1500 Greenbugs 1400 1300 1200 s per Pl s per 1100 dd 1000 900 800

e Aphi 700 gg 600 500 400

Avera 300 200 100 0 6/97 1/97 3/98 0/99 9/99 8/00 0/95 5/95 4/96 /1/97 /5/98 /3/96 22 11 22 33 11 11 22 22 11 88 88 77 7/ 8/ 8/ 6/ 9/ 6/ 6/ 8/ 7/ Other Irrigated: Oldham Co. 1994, Parmer Co. 1995

2000 1900 1800 1700 Corn Leaf Aphids nt 1600 aa 1500 Greenbugs 1400 1300

per Pl 1200 ss 1100 1000 900 800 e Aphid 700 gg 600 500 400

Avera 300 200 100 0 2/9 /94 1/9 /95 /95 11 88 11 33 77 7/ 8/ 7/ 8/ 9/ Other Rainfed: Gray Co. 1994, Parmer Co. 1995

2000 1900 1800 1700 nt 1600 Corn Leaf Aphids aa 1500 1400 Greenbugs 1300

per Pl 1200 ss 1100 1000 900 800 e Aphid 700 gg 600 500 400

Avera 300 200 100 0 2/9 /94 1/9 /95 /95 11 88 11 33 77 7/ 8/ 7/ 8/ 9/ 10000 All Fields

1000 /plant yy

100 bug densit nn

10 Peak gree Peak

1 -25 -20 -15 -10 -5 0 5 10 15 20 25 DditifDays deviation from sorghum hbtth boot stage when cornl eaf ap lfhidhids average100 per 100lt 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. S. graminum peak, Day 229

First S. graminum , Day 215

Predator peak, Day 212

R. maidis peak, Day 202

First predator egg, Day 200

R. maidis = 100, Day 195

Seasonal Occurrence of Aphids and Predators in Irrigated Sorghum Fields (95% CI)

Sorghum Boot, Day 195 188 190 192 194 196 198 200 202 204 206 208 210 212 214 216 218 220 222 224 226 228 230 232 234 236 238 Day of the Year Ye ar - 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. 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 195 188 190 192 194 196 198 200 202 204 206 208 210 212 214 216 218 220 222 224 226 228 230 232 234 236 238 Day of the Year Ye ar - Ημέρα του έτους

The seasonal events in rainrain--fedfed 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. 1.75

Coccinellid Adults and Larvae 1.50 Coccinellid Egg Masses

1.25

1.00 nellids 0.75 Cocci

0.50

0.25

0.00 17 24 31 14 21 28 15 22 29 13 20 27 10 9/7 7/6 8/3 // // // // // // 6/1 6/8 // // // // // // // 8 8 8 9 9 9 6 6 6 7 7 7 8

The typical predator adult and egg mass abundance profile in grain sorghum, average of irrigated and rainrain-- fed fields, 19881988--2000.2000. 350 1.75 Corn Leaf Aphid 300 Coccinellid Adults and Larvae 1.50 Cocc ine llid Egg Masses 250 1.25 Cocci 200 1.00 ids n hh ellids

Ap 150 0.75

100 0.50

50 0.25

0 0.00 17 24 31 14 21 28 15 22 29 13 20 27 10 9/7 7/6 8/3 // // // // // // 6/1 6/8 // // // // // // // 8 8 8 9 9 9 6 6 6 7 7 7 8

TheOverlay typical of corn predator leaf aphid adult abundance and egg mass for the abundance same fields profileand years. in grain These sorghum, prey seem average to explain of irrigated the first predator and rain-fedpeak, but fields, not the 1988-2000. second. 350 1.75 Greenbug 300 Coccinellid Adults and Larvae 1.50 Cocci ne llid E gg M asses 250 1.25 Cocci 200 1.00 ids n hh ellids

Ap 150 0.75

100 0.50

50 0.25

0 0.00 17 24 31 14 21 28 15 22 29 13 20 27 10 9/7 7/6 8/3 // // // // // // 6/1 6/8 // // // // // // // 8 8 8 9 9 9 6 6 6 7 7 7 8

Overlay of greenbug abundance for the same fields and years. These prey seem to explain the second predator peak, but not the first. 350 1.75 Corn Leaf Aphid 300 Greenbug 1.50 Cocci ne llid Adu lts an d Larvae 250 Coccinellid Egg Masses 1.25 Cocci 200 1.00 ids n hh ellids

Ap 150 0.75

100 0.50

50 0.25

0 0.00 17 24 31 14 21 28 15 22 29 13 20 27 10 9/7 7/6 8/3 // // // // // // 6/1 6/8 // // // // // // // 8 8 8 9 9 9 6 6 6 7 7 7 8

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? 350 1.75 Combined Aphids 300 Coccinellid Adults and Larvae 1.50 Cocc ine llid Egg Masses 250 1.25 Cocci 200 1.00 ids n hh ellids

Ap 150 0.75

100 0.50

50 0.25

0 0.00 17 24 31 14 21 28 15 22 29 13 20 27 10 9/7 7/6 8/3 // // // // // // 6/1 6/8 // // // // // // // 8 8 8 9 9 9 6 6 6 7 7 7 8

If corn leaf aphid and greenbug are looked at as a continuum of prey rather than distinct occurrences, the predator profile makes more sense. 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 tiiime t on aphid a bun dance at samp ling t ime t-2. This “loo k bac k” approac h was employed using various steps back, with tt--22 being found to be the most relevant. Prior to tt--2,2, the predictions were too weak, and at tt--11 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 blibelieve thtththat these are key componen ts to und ers tandi ng the sys tem an d open a dditiona l avenues for future research. Correlation Coefficients for Aphids, Coccinellids, and Coccinellid Eggs

Rainfed Irrigated Predator First Predator First peak egg peak egg R. maidis peak 0.693 0.677 0.663 0.705 Prob. 0.084 0.095 0.005 0.007 S. graminum peak 0.470 0.167 0.638 0.316 Prob. 0.287 0.721 0.008 0.293 R. maidis =100 0.865 0.909 0.677 0.705 Prob. 0.012 0.005 0.004 0.007

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 siggynificantly correlated to first e ggggg in irrigated fields. However , these numbers can onl y 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. Simple Linear Regressions of Aphid Variables on Coccinellid Peak Abundance

Equation R2 p Interpretation All fields considered, irrigation regime not separated out

C=29.5+0.033SG 0.19 0.010 ~ 30 SG for 1 ladybeetle C=20.1+0.034A 0.20 0.009 ~ 30 aphids for 1 ladybeetle C=20.4+0.034SG+0.037RM 0.20 0.035 ~ 37 RM or 34 SG for 1 ladybeetle C=11.3+24I+0.037A 0.21 0.027 Effect of RM>=100 by boot stage Paired field analyses, (1 irrigated, 1 rain-fed field) , 10 comparisons, 20 fields C=10.8+0.024SG 0.77 0.024 ~ 24 SG for 1 ladybeetle C=4+0.025A 0.77 0.025 ~ 25 aphids for 1 ladybeetle C=6C=6--(5*I)+0.025A(5*I)+0.025A 0.78 0.000 ~ 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 35

30 Greenbugs alone All fields 2 25 R =0.77, p =0.024 m of row m of

55 Any aphid 20 All fields R 2 =0.77, p =0.025 15 ccinellids/1 oo

10 Peak C Peak

5

0 0 100 200 300 400 500 600 700 800 900 1000 Ahid/lAphids/plan t

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

Peak Coccinellids = 6 - (5*I) + 0.025 aphids 30 2 R =0. 78, p =0. 000 Irrigated Fields

25 5 m of row of 5 m 20

15 occinellids/1 Rainfed Fields CC

10 Peak Peak

5

0 0 100 200 300 400 500 600 700 800 900 1000 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. 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/pl ant b y th e b oot st age of sorgh um prob abl y result s i n f ew cocci nellid s ovipositing, and greenbugs not being subjected to predation sufficient to keep their numbers below economically damaging levels. 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 seemilhd“lfhb”ihingly handy “rule of thumb” is that green bug bililbiological contro lbl 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. 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 (R2).

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 greenb ug onl y regressi on hi nts at a hi gh er cocci ne llid a bun dance be ing 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 coccine llid pea k. Results and Conclusions

Bothoth 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 sideside--byby side comparisons o fiif irrigate d an d ra ifdinfed grai n sorg hum fildfields, t here are st ill questions that need to be answered. The results point to a need to thoroughly assess climatic conditions, and perhaps look at the role nonnon--coccinellidcoccinellid 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 a ll, the gra in sorg hum /ap hid/pre da tor ecosys tem rema ins an in teres ting and mysterious place that has been a joy to work in over the years. Pertinent Historical Literature

Kring, T. J., and F. E. Gilstrap. 1983. Within field distribution of greenbug (Homoptera: ) and its parasitoids in Texas winter . J. Econ. Entomol. 76: 57-62.

Kring, T. J. and F. E. Gilstrap. 1984. Efficacy of three natural enemies of grain sorghum aphids (Homoptera: Aphididae). J. Kan. Entomol. Soc. 57: 460-467.

Kr ing, T. J., F. E . Gil st rap, and G . J . Mi ch el s, J r. 1985 . Ro le o f in digenous coccinellids in regulating greenbugs (Homoptera: Aphididae) on Texas grain sorghum. J. Econ. Entomol. 78: 269-273.

Kring, T. J. and F. E. Gilstrap. 1986. Beneficial role of corn leaf aphid, Rhopalosiphum maidis (Fitch) (Homoptera: Aphididae) in maintaining Hippodamia spp. (Coleoptera: Coccinellidae) in grain sorghum. Crop Protection. 5 : 125 -128.

Rice, M. E. and G. E. Wilde. 1988. Experimental evaluation of predators and ppppggg(pp)garasitoids in suppressing greenbugs (Homoptera: Aphididae) in sorghum and wheat. Environ. Entomol. 17: 836-841. Σας ευχχραριστώ για την καλή προσοχή σας!

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