The vertical distribution of green peach aphids and its effect on a model quantifying the relationship between green peach aphids and a predator

1981) MACK AND SMILOWITZ: GPA DISTRIBUTION 345

THE VERTICAL DISTRIBUTION OF GREEN P E A C H APHIDS 1 AND ITS EFFECT ON A MODEL QUANTIFYING THE RELATIONSHIP

BETWEEN GREEN P E A C H APHIDS AND A P R E D A T O R 2

T.P. Mack and Z. Smilowitz ~

Abstract

The vertical distribution of green peach aphids (GPA) on potato plants was studied to estimate its impact on a model simulating the effects of a predator on GPA populations. This model is based on laboratory studies of a ladybird beetle feeding on GPA that was placed exclusively on the bottom leaf o f a three leaf stem section. The model predicts the impact of Coleomeg- ilia maculata (DeGeer) adults and third instar larvae on GPA populations over a range of temperatures and GPA densities.

The vertical distribution of GPA in a potato field and the effects of different levels of aldicarb on this distribution were determined by counting all GPA on the upper, middle, and lower thirds of a stem in situ. A one leaf sub-sample was taken from each stem section as a comparison.

The vertical distribution of GPA changed with aldicarb dose. Most GPA were found on the lower third of stems from plots treated with the lowest aldicarb doses. However, most GPA occurred on the upper third of the stems from plots treated with the highest aldicarb doses. This distribution changed midway through the season until most GPA occurred on the bottom third of the stems.

C. maculata adults and third instar larvae preferentially search the upper and lower thirds of potato plants. This suggests that C. maculata would be an effective early season predator, and that our model should over-predict the effect of C. maculata on GPA populations late in the season.

Resumen

La distribuci6n vertical del Afido verde del duraznero (GPA) in plantas de papa fu6 estudiada para estimar su impacto en un modelo que simulaba los efectos de un predator sobre poblaciones del ~fido verde. Este modelo est6 basado en estudios de laboratorio realizados con "mariqui tas" alimen- t6ndose de 6fidos verdes colocados 6nicamente sobre la hoja mas inferior de una secci6n de tallo con 3 hojas. E1 modelo predice el impacto de adultos

~Myzus persicae (Sulzer) (Homoptera: Aphididae). 2Authorized for publication on 6/24/80 as paper no. 6011 in the journal series of the Penn- sylvania Agricultural Experiment Station. 3Department of Entomology, The Pennsylvania State University, University Park, PA 16802. Received for publication August 14, 1980. Current address of senior author: Zoology-Entomology Department, Auburn Univ., Auburn, AL 36849. KEY WORDS: Myzus persicae, Coleomegilla maculata, potato plants, vertical distribution.

346 AMERICANPOTATOJOURNAL (Vol. 58

y larvas del tercer estadio de Coleomegilla malucato (De Geer) sobre poblaciones del ,~tfido a diferentes temperaturas y densidades.

La distribucibn vertical del/~fido verde en un campo de papa y el efecto de diferentes niveles de aldicarb fu6 determinado por contadas de todos los ~tfidos en los tercios superior, medio e inferior de un tallo "in situ". Una hoja de cada tercio fu6 tomada como sub-muestra por comparacibn.

La distribucibn vertical del/tfido verde vari6 con la dosis de aldicarb. La mayoria de/ffidos fueron encontrados in el tercio inferior de los tallos procedentes de parcelas tratadas con las dosis m~ts bajas de aldicarb. Sin embargo, la mayorta de/ffidos se encontraban en el tercio superior de los tallos procedentes de parcelas tratadas con las dosis m[ts altas de aldicarb. Esta distribuci6n empez6 a cambiar a mediados de la campafia hasta que a la mayoria de 6fidos se encontraban en el tercio inferior de los tallos.

Adultos y larvas del tercer estadio de C. maculata prefieren los tercios superiores e inferiores de las plantas de papa. Esto sugiere clue C. maculata podria ser un predator efectivo a los inicios del cultivo y que nuestro modelo podria sobre estimar el efecto de C. maculata en poblaciones del ~fido verde en los periodos finales del cultivo.

Introduction

Mack and Smilowitz 4 have developed models that simulate the impact of Coleomegilla maculata s (DeGeer) adults and third instar larvae on Myzus persicae (Sulzer), the green peach apid (GPA). These models are based on laboratory studies of C. maculata feeding on GPA that were placed exclusively on the bottom leaf of a three leaf potato stem section. This cut section was small enough so that the predators could search the entire section many times in the 24 hr that the predators were allowed to feed. Thus, an assumption of these models was that the predators could find and thoroughly search the most infested areas of the stem section. This assumption is probably not correct for C. maculata searching for GPA in a potato field, since it is very unlikely that C. maculata could search an entire potato plant many times in 24 hr. The vertical distribution of GPA and the searching strategies of C. maculata would play important roles in determining the effectiveness of the laboratory models in describing field populations. For example, the models would over estimate the effectiveness of C. maculata if the vertical distribution were such that few aphids occurred in areas that C. maculata regularly searched. The goal of this study was to determine the effects of the vertical distribution of GPA on the laboratory models predicting the impact of C.

4Mack, T.P. and Z. Smilowitz. 1981. Using temperature-mediated functional response models to predict the impact of Coleomegilla maculata (DeGeer) adults and third instar larvae on green peach aphids. Accepted for publication in Environ. Entomol. SColeoptera: Coccinellidae.


maculata adults and third instar larvae feeding on the aphids. Two questions need to be answered to achieve our goal:

a) What is the vertical distribution of GPA occurring on field grown potato plants?

b) Do C. maculata larvae and adults normally find and search the areas where most GPA are likely to be found?

The remainder of this paper is directed to answering these questions.

Methods and Materials

This study was conducted at The Pennsylvania State University Agri- cultural Farm at Rock Springs, Pennsylvania in 1979. Foundation potato (Solanum tuberosum L. var Katahdin) seed pieces were mechanically planted 23 cm apar t in 86 cm wide rows. Standard weed and disease control practices were followed (1).

Experimental Design - A randomized complete block design was em- ployed, containing four blocks (replicates) and three treatments per block. Each 16 row x 56.4 m treatment plot corresponded to a specific level o f aldicarb 15G insecticide applied in the furrows at planting. The three aldicarb levels were: 1.12, 1.68, and 3.36 kg AI /ha .

Aphid sampling occurred weekly from July 9 to August 20, 1979. Aphids other than GPA were rarely found. The time of day that sampling occurred and the personnel that sampled a given plot were randomized each week to decrease the likelihood of systematic errors in the data. A single row from every plot was located by drawing a random number each week for sampling. Once sampled, this row was never selected again. The rows adjacent to the sample row were not sampled for at least 13 days to allow the plants to re- cover f rom any injuries that may have occurred. Twenty potato plants were randomly selected f rom the sample row, and a stem was selected f rom each plant. These stems were divided into an upper, middle, and lower section, and the GPA on the foliage f rom each section examined in the field were re- corded. A leaf was randomly selected f rom the three sections f rom the same plants and the aphids counted so that a three leaf aphid sample (2, 5) could be compared to the three section aphid sample. The user of a three leaf sampling technique assumes that the GPA density on a leaf is approximately equal to the density on the stem section. In making this assumption the user also assumes that the GPA density on the shoot apex and young leaves, lateral branches, leaf stipules, and the stem wings is approximately equal to the aphid density on the stem section, since these areas are not sampled in a three leaf sample.

Upper, middle, and lower leaf and stem areas were determined from four plants / t reatment on 7/26/79 and 8/3/79. A leaf area meter was used to determine the leaf and stem areas. These areas were determined so that aphid densities (no . /cm 2) could be used in an analysis o f variances. GPA

348 AMERICAN POTATO JOURNAL (Vol. 58

densities were loglo (x + .000001) transformed before analysis because a Kol- omogorov-Smirnov test (4) on untransformed data indicated that the resid- uals were not normally distributed. The transformed densities on both dates were analysed as a split-split-plot (8) with subsampling. Aldicarb levels, sample type (stem or leaf), and plant positions (upper, middle, or lower) were all considered to be fixed effects. Duncan's multiple range test was used on the plant position, sample type interaction means to determine if significant changes occurred.

Results

The vertical distribution of GPA changed with aldicarb level and sample date. Most GPA were found on the foliage from the lower two-thirds of the stem lengths (Fig. la) and on the middle or lower leaves (Fig. ld) from plots treated with the lowest aldicarb dose. Similar results were obtained by Anscombe (2), who stated that few aphids were normally found on top leaves. However, most GPA were found on the upper third of stems sampled from July 9-30 in plots treated with the two higher aldicarb levels (Fig. lb, lc). Many GPA were found during this time on the shoot apex and young leaves. These results concur with those reported by Bradley (5). This distribution changed after July 30 until more GPA occurred on the lower two- thirds of the stems and on the middle or lower leaves.

Analysis o f Variances Results. ~ The GPA density analysis for the 7/30/79 data indicated that the sample type. plant position interaction was significant (p < .09), so no main effects could be analysed (14). A Duncan's multiple range test on the sample type,plant position means for each aldicarb level (Table 1) indicated that all of the sections had higher GPA densities than the leaf samples (p_<. 10). We believe this was caused by a higher GPA density on the lateral branches and leaf stipules than on the primary leaves, since these areas would not normally be sampled in a three leaf sample. The upper and/or lower stem density ranked as the highest density for all of the aldicarb levels. Thus, most GPA occurred on the upper and lower thirds of the plants. There are many factors that may have contributed to a higher GPA density on the upper and lower stem sections. Two possible mechan- isms are: (a) GPA that occurred on the terminal rosettes would be very ex- posed to winds. GPA that were removed by the wind would crawl to a plant and probably stay on the first leaves they encountered, which would be the lowest leaves. (b) Coccinellid predators have been shown to spend a significant amount of time searching upper plant parts (3). They have also been known to increase the dispersal of aphids (12). Dixon (6) stated that natural enemy attacks caused pea aphids to drop from plants. Similar attacks by C. maculata on GPA occurring on upper plant parts may have caused GPA to drop from the plant and crawl back to the lowest leaves.

Aldicarb level appears to have had a definite effect on the vertical distribution of GPA from stem sections. The lower stem section mean was the


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FIG. 1. Mean number of M. persicae found on potato plant samples from July 9-August 20, 1979. positions: �9 lower, �9 middle, 0 upper. Legend: 1.12 kg Al/ha aldicarb: (A) stem samples, (D), leaf samples.

1.68 kg AI/ha aldicarb: (B) stem samples, (E) leaf samples. 3.36 kg AI/ha aldicarb: (C) stem samples, (F) leaf samples.

largest GPA density for the 1.12 kg AI/ha aldicarb plots. This was significantly (p_<. 10) larger than both the upper and middle stem GPA densities, which were not significant from each other. At 1.68 kg AI/ha aldicarb the GPA densities from the upper and lower stems ranked at the largest means. The aphid density from the middle stem was significantly lower than the upper and lower stem densities. Finally, at 3.36 kg AI/ha aldicarb the GPA


TABLE 1. - - July 30, 1979 vertical distribution o f green peach aphid densities (no./cm2).

Aldicarb" Sample Type Plant Position Mean b

1.12 stem 1.12 stem 1.12 stem 1.12 leaf 1.12 leaf 1.12 leaf 1.68 stem 1.68 stem 1.68 stem 1.68 leaf 1.68 leaf 1.68 leaf 3.36 stem 3.36 stem 3.36 stem 3.36 leaf 3.36 leaf 3.36 leaf

upper middle lower upper middle lower upper middle lower upper middle lower upper middle lower upper middle lower

-4.408(.00259) B - 4.308(.00278) B -4.129(.00794) A -5.539(.00190) FG - 4.950(.00408) C -4.958(.00563) C - 5.262(.00088) DE - 5.520(.00029) FG -5.122(.00072) CD - 5.748(.00079) GH - 5.758(.00050) GH - 5.759(.00047) GH - 5.383(.00045) EF - 5.717(.00018) GH - 5.575(.00038) FG - 5.904(.00018) H -5.909(.00011) H - 5.756(.00060) GH

*kg AI/ha. bMeans determined from 80 log,o (X + .000(~1) observations on July 30, 1979. Numbers in parentheses are the untransformed means. Means followed by the same letter are not significantly different (t~ = .10) according to Duncan's multiple range test. An c~ = .10 was used because the consequences of a Type I error were not considered to be absolutely critical, as outlined in Little and Hills (8).

density f rom the upper stems was s ignif icant ly larger t han either the middle

or lower stem densities. Thus , the p ropor t ion of the G P A density on the upper stems increased as the level of a ldicarb increased.

Aldicarb levels had less of an effect on the vertical d is t r ibut ion of GPA from the three leaf samples. The G P A density on the upper leaves f rom 1.12 kg A I / h a a ldicarb plots was s ignif icant ly lower (p_< .10) than that on the

lower or middle leaves. These results concurred with the f indings of other researchers (7, 11, 13) who have used the three leaf sampl ing technique. This vertical d i s t r ibu t ion of G P A densities f rom the leaves agreed with the 1.12 kg

A I / h a a ldicarb stem samples, a l though the leaf densities were all lower than the stem densities. However, the vertical d is t r ibut ions f rom the leaves and stems for the 1.68 and 3.36 kg A I / h a aldicart~ plots did no t agree. The upper leaf densities f rom the 1.68 and 3.36 aldicarb plots were not significantly greater than the middle leaf GPA densities as they were for the stem samples.

This difference in GPA density between upper stems and upper leaves con- forms with our field observat ions of higher GPA densities on the shoot apex and young leaves, which are no t sampled in the three leaf sampl ing method.

One year ' s observat ions of a GPA colony reared on Ka tahd in variety pota to


plants in large growth chambers have also indicated that the shoot apex and young leaves can become heavily infested with GPA. The shoot apex and young leaves of a 'Katahdin ' potato plant appear to be more susceptible to GPA attack because it is more tender tissue than a mature leaf. This would account for the higher densities observed on such tender tissue as the shoot apex, young leaves, lateral stipules, and small lateral branches. We believe that the user of a three leaf sampling technique should not assume that these tender tissue areas have the same aphid density as mature leaves. Further sampling of at least some of these areas should be conducted.

The analysis of variances results for the 8/6/79 data indicated that no main effects or simple interactions could be statistically analysed since the aldicarb.sample type .p lan t position interaction was nearly significant ( p < .11). A study of this interaction indicated that at all three aldicarb levels the GPA densities from the stem sections were greater than the densities f rom the leaf samples. This agrees with the 7/30/79 analysis results. However, the means from the lower and middle stem sections were greater than the means from the upper section. This was true for all three aldicarb levels, and conflicts with the 7/30/79 analysis. Thus, the vertical distribution of GPA appears to have changed during the season.

With this in mind it is now possible to study the search strategies em- ployed by C. maculata. Rinker et a13 analysed the time C. maculata third instar larvae spent on an artificial stem designed to be similar to a 50 cm potato stem. They found that larvae starved for 48 hr spent significantly more time (Table 2) on the upper position than satiated larvae. Starved larvae also spent most of their total time on the upper and lower positions of

TABLE 2. - - Mean time C. maculata third instar larvae spent on plant posit ions (sec/cm2) ~

Plant Position Satiate& Starved

Lower 84.97:t:24.8 A 64.15+ 13.4 A Middle 18.78+ 18.3 A 16.58+ 5.9 A Upper 9.02• 12.5 B 54.12• A

*From the unpublished manuscript entitled "Quantification of time on vertical and horizontal surfaces by the third instar Coleomegilla maculata (DeGeer) (Coleoptera: Coccinellidae)" by D. Rinker, M. Hutton and V. Starner. Used with permission of the authors. It is available from Z. Smilowitz, Department of Entomology, The Pennsylvania State University, University Park, PA 16802. bMeans in rows followed by the same letter ale not significantly different (ct = .05) using Stu- dent's t-test.

6Rinker, D.L., M.G. Hutton, and V. Starner. 1980. Quantification of time on vertical and horizontal surfaces by third instar Coleomegilla maculata (DeGeer)(Coleoptera: Coccinellidae). Unpubl. manuscript. 17 pp.


the artificial stem. Thus, starved C. maculata third instar larvae searched areas that coincided with the vertical distribution o f GPA early in the season.

Most C. maculata adults seem to occur on the lower third o f potato plants (9). However, we have observed many adults searching the upper third of plants early in the morning (10). Apparently, C. maculata adults also search both the upper and lower thirds of plants. This suggests that C. maculata adults would be effective early predators because the areas they search coincide with the vertical distribution of GPA. Once the vertical distribution, of GPA changes so that most GPA occur on the lower third o f potato plants, C. maculata adults and larvae should not be very effective predators, if the search behavior of C. maculata did not change to account for this GPA distribution change. Thus, our simulation models should over-predict the effects of C. maculata on GPA populations later in the season, since the predators would be spending a large amount of time searching areas with low GPA densities.

Acknowledgments

We gratefully acknowledge the assistance of J. Dill, S. Homan, T. Houston, G. Hanley, B. Lucas, J. Brietzman, and K. Thorenson in data collection. We are also indebted to B.A. Bajusz for her continued assistance in data analysis. Finally, we thank R. A. J. Taylor, R. Craig, L. Hull, and F. Williams for critically reviewing the manuscript.

Literature Cited

1. Anonymous. 1978. Agronomy Guide. The Pennsylvania State University, Extension Service Publ. No. 35M1276.

2. Anscombe, F.J. 1948. On estimating the population of aphids in a potato field. Ann. Appl. Biol. 35:567-71.

3. Banks, C.J. 1957. The behavior of individual coccinellid larvae on plants. Brit. J. Anim. Behav. 5:12-24.

4. Barr, A.J., J.H. Goodnight, J.P. Sail, W.H. Blair, and D.M. Chilko. 1979. SAS User's Guide: 1979 edition. SAS Institute, Inc., Raleigh, NC 494 pp.

5. Bradley, R. H.E. 1952. Methods of recording aphid (Homoptera: Aphididae) populations on potatoes and the distribution of species on the plant. Can. Entomol. 84:93-102.

6. Dixon, A. F.G. 1959. An experimental study of searching behavior of the predatory coccinellid beetle, Adalia biputictata (L.). J. Anita. Ecol. 8:259-81.

7. Jacob, F.H. 1941. The overwintering ofMyzuspersicae (Sulz.) on Brassica in North Wales. Ann. Appl. Biol. 28:119-24.

8. Little, T.M. and F.J. Hills. 1972. Statistical methods in agricultural research. UCD Book Store, University of California, Davis, CA. 242 pp.

9. Mack, T. P. and Z. Smilowtiz. 1977. Nocturnal and diurnal movements of beneficial insects in a potato field. J. NY Entomol. Soc. 85:189.

10. Mack, T.P. and Z. Smilowitz. 1980. Development of a green peach aphid natural enemy sampling procedure. Environ. Entomol. 9:446-451.


11. Norris, D.O. and J.G. Bald. 1943. Transmission of potato virus disease. 2. The aphis population of potatoes at Canberra during 1940-41. Australian Coun. Sci. Ind. Res. Bull. 163.

12. Roitberg, D.B., J .H. Myers, and B.D. Frazer. 1979. The influence of predators on the movement of apterous pea aphids between plants. J. Anim. Ecol. 48:111-22.

13. Shands, W.A., G.W. Simpson, and C. G. Gordon. 1971. Growth characteristics of potato plants useful in studies of population dynamics and biological control of aphids. Amer. Pot. J. 48:439-49.

14. Steel, R. G. D. and J. H. Torrie. 1960. Principles and procedures of statistics. McGraw Hill Book Co., Inc., New York, NY. 481 pp.

Documents

The vertical distribution of green peach aphids and its effect on a model quantifying the relationship between green peach aphids and a predator