Effects of biological control agents and insecticides on the population development of Myzus nicotianae Blackman (Homoptera: Aphididae) on tobacco

Agriculture Ecosystems & Environment ELSEVIER

Agriculture, Ecosystems and Environment 52 (1995) 57-64

Effects of biological control agents and insecticides on the population development of Myzus nicotianae Blackman (Homoptera: Aphididae) on tobacco D.P. Lykouressis, G.V. Mentzos Laboratory of Agricultural Zoology and Entomology, Agricultural Universityof Athens, Athens, GR-11855, Greece

Abstract

The phenology of Myzus nicotianae Blackman showed that alates appear early in the seedbed, which implies anholocycly. The aphid population developed slowly for at least 4 weeks after transplanting, then increased nearly to the end of the growing season. Spraying, at the onset of rapid aphid increase, was very effective in controlling the aphid population. Aphidiid parasitoids and fungal diseases were the main biological mortality agents with coccinellids, syrphids and chrysopids present in low numbers. Aphid populations were higher on upper than on lower leaves, the reverse being true for mummies. The number of parasitoids was therefore reduced by removal of leaves. Agricultural practices which could contribute to the effectiveness of parasitoids and fungal diseases are discussed.

I. Introduction

The green peach aphid, Myzus persicae (Sulzer), is an important pest of Nicotiana tabacum L. in several tobacco growing areas of the world. It was first reported on tobacco in the United States in the 1940s (Dominick, 1949; Chamberlin, 1958). Blackman (1987), used morphometric characters to describe a tobacco form of M. persicae (Myzus nicotianae Blackman). Morphological differences between M. persicae and M. nicotianae are slight, and require canonical variate analysis with 11-14 characters to distinguish them. Blackman and Spence (1992) however, found that the two taxa can be separated by electrophoresis on cellulose acetate using glutamate oxaloacetate transaminase. This species has green and red colour forms, the latter being predominant in eastern Asia (Takada, 1986). In the USA the red form was first noticed in North Caro0167-8809/95/$09~50 © 1995 Elsevier Science B.V. All rights reserved SSDIO 1 67-8 8 0 9 ( 9 4 ) 0 9 0 1 0 - 5

lina in 1985 (Lampert and Dennis, 1987) and became predominant in populations in North Carolina, Virginia and Maryland in 1986 (Blackman, 1987). Reed and Semtner ( 1991 ) have shown that in both morphs of M. nicotianae, the optimal temperature for development was 25°C. Blackman and Takada (1975) found that green peach aphids with autosomal 1,3 translocation had high levels of esterase activity. Harlow et al. (1991) identified in cultures ofM. nicotianae from North Carolina, two karyotypes, one with 12 chromosomes with a normal configuration and the other with 12 chromosomes with a 1,3 autosomal translocation. Large numbers of aphids cause wilting of leaves and reduction in yield and quality because of the premature ripening of the lower leaves. Damage to tobacco results from direct feeding, from mould developing on honeydew, and from plant virus transmission (Kennedy et al., 1962; Van Emden et al., 1969; Mistric and Clark, 1979; Throne and Lampert, 1985).

58

D.P. Lyko.ressis, G. V. Mentzos / Agriculture, Ecosystems and Environment 52 (1995) 57-64

Myzus nicotianae is regarded as a serious pest of tobacco in Greece, together with Epithrix hitripennis (Melsheimer) (Lykouressis, 1991), against which chemicals are used. Seasonal abundance and within-plant distribution of M. nicotianae was studied by Lampert (1989) on fluecured tobacco. Semtner (1984) looked at the effect of transplantation date and of two predators, the coccinellid Hippodamia conzergens Guerin-Meneville and the hemipteran Jalysus wickhami van Duzee, on aphid abundance. Little is known on natural enemies and pathogens of M. nicotianae in the field. This paper reports studies on the abundance and effects of parasitoids on M. nicotianae, and ways to enhance their action.

2. Materials and methods

2.1. Studyplots To study the phenology and population dynamics of M. nicotianae, samplings were carried out during 1990-1991 in a tobacco field located at Nea Avorani, 6 km from the town of Agrinio (Aitoloakarnania). The tobacco was a local variety called "tsempeli" which is widely planted. The climate is typically Mediterranean with high summer temperature and high relative humidities in spring and autumn. The mean temperatures in June and July 1990 were 25.2°C and 28.9°C, respectively, and 25.2°C and 26.5°C in 1991. The mean relative humidity

2 (a)

L I

{d)

1,6

i

e.o,*

~

l

e.e2

I I

11

21

A~:r i

1

1

'.'.~'/

11

21

Ap~ i i

i Ma v

2.4!

8.o~ (b)

(e)

e-

>B,~2

.~ l . a

l

o i

11

:d:

el

[-

i °. I

I.!J ,:

<

m

' 1

11

April

mill 21

/ 1 ~,~, , ,

(c)

.~.

/

15 t o.1[

ll 1

11

,it

~i

?I

I I.~~,

Fig. 1. Mean ( + SE) number of M. nicotianae per seedling in the seedbed in 1991: (a) apterous nymphs; (b) fourth instar alate nymphs; (c) apterous adults; (d) alate adults; (e) total population.

D.P. Lykouressis, G. V. Mentzos /Agriculture, Ecosystems and Enviromnent 52 (1995) 57-64

in June and July 1990 was 53% and 52.5%, and 53% and 58.8% in 1991. July 1990 was exceptionally hot, July 1991 being normal. Total rainfall during June, July and August 1990 and 1991 was 61.9 mm and 79.1 mm, respectively. Rainfall during the summer months in 1990 was low compared with 1991. Sampling commenced on 30 May 1990, 10 days after tobacco transplanting and was repeated every 10 days. The phenology of M. nicotianae was studied in a plot (A) of approximately 500 m 2 ( 3 0 r o w s , 40 cm apart, 34 m long) located at the edge of the tobacco field. Sampling in 1991 started from the seedbed on 1 April and continued after transplanting at 10 day intervals. The seedbed was divided into four blocks of 20 m × 1 m each.

~

59

The population dynamics ofM. nicotianae was studied in 1991 from the seedbed and continued in the field in two contiguous plots, A (as for 1990) and B (500 m 2, 30 rows × 34 m). Plot A remained untreated, and plot B was treated twice, on 31 May, after sampling with endosulphan, and on 12 July with ethiofencarb. Sowing occurred on 25 February and transplanting on 4 May. Plants were placed 12-15 cm apart. Plots were hoed on 24-25 May, irrigated on 29 May, 9, 17 and 26 June, and 15 July, and plants were topped on 4 July. Picking of the lowest three to four leaves occurred on 8, 18 and 25 June, and of the top leaves on 7, 14 and 27 July. Plants in both plots were sprayed on 31 May againstPeronospora tabacina with metalaxyl and mancozeb. • Upper [] Lower"

Upper Lower

11

(d)

.

~ e.e L

z

all

,~

11

21

31

le

i

o |.|

z ao

30

le

e

2e

•

11

-21

3I

lO

2e

30

Upper Lower

lO

20

• []

Upper

lO

20

Lower

3~ (b)

41-

41-

2

4

~ 2e

~e.5 0 11

21

31

1o

2e

3e

Is

20

• []

Upper Lower'

11

21

31

lO

20

30

e~

(el

i4i

i

e

-|

i 11

21 ?:

31

Io

20

|1 30

le

2(]

~r:

Fig. 2. Mean ( + SE) number of M. nicotianae per leaf from the upper and lower halves of tobacco plants in the treated plot B (arrow indicates spraying date) in 1991: (a) apterous nymphs (b) fourth instar alate nymphs; (c) apterous adults; (d) alate adults; (e) total population.

60

D.P. Lykouressis, G. I/. Mentzos / Agriculture, Ecosystems and Environment 52 (1995) 57-64

2.2. Sampling, treating and counting of aphids The sampling unit was a leaf; it was a whole seedling in the seedbed. In 1990, sampling after transplanting was carried out on 30 May, 9, 19 and 29 June and 9, 19 and 29 July. A total of 25 samples was taken, each being a leaf from the upper half of a tobacco plant. Twenty-five seedling samples were taken from the seedbed in 1991 on 1, 11, 21 April and 1 May at a distance of 3 m along each block. Leaf sampling was carried out on 11,21 and 31 May, 10, 20 and 30 June and 10 and 20 July 1991. From each plot, 25 samples were taken: the first at the centre of

the plot and the others 39 m apart down the rows. Each sample comprised two leaves, one from the upper and one from the lower half of each plant, except on 11 May, when one leaf only was cut from each plant because of their size. Each leaf was placed in a plastic bag and kept at 5°C for examination under a stereo microscope. Live aphids were preserved in a 2: 1 ratio of 90-95% ethyl alcohol and 75% lactic acid (Eastop and Van Emden, 1972). Diseased aphids were counted per leaf sample. Mummies were counted and kept separately in a small plastic vial to allow for adult emergence. Other natural enemies such as coccinellids, syrphids and

• ~r

• ~r

[] L o w e r

[] L o w e r

i 4 ~12e

++:

._t 11

21

31

10

l 2e

3e

le

2e

•

Upper

i:

_ 21

31

le

2e

i. 30

2e

• Upper [] Lower

[] Lower

il

le

+'

~

2se

~ 15e ~lee

i

-

eL 11

21

31

le

,11,,

20

t 3e

le

J z:h

20 "u L

• []

~ .L__ L . _ 11

2x :-l~v

31

10

2e J,:~/

3e

le

2e ~ l~,,

Upper Lower

+::I [L )° °I

t

._| 11

RI "

31

lO

20 ]u-/,

30

18

2@

uL/

Fig. 3. Mean ( + SE) number of M. nicotianae per leaf from the upper and lower halves of tobacco plants in the untreated plot A in 1991: (a) apterous nymphs; (b) fourth instar alate nymphs (c) apterous adults; (d) alate adults; (e) total population.

DmP. Lykouressis, G. V. Mentzos / Agriculture, Ecosystems and Environment 52 (1995) 57-64

chrysopids were counted and any adults present identified to species. Preserved aphids were sorted into apterous and alate adults, fourth instar alates, and first, second, third and fourth apterous instars. Several samples from both years were sent for confirmation to the Natural History Museum, London; all were identified as M. nicotianae. Analysis of variance was done on transformed data (Xtra. s -- X ~ 0.5), using Student-Newman-Keul's test. Means were tested for significance by the TukeyKramer test at the 5% and 1% levels of significance. •

61

3. Results

3.1 Phenology ofM. nicotianae in 1990 A small population o f M . nicotianae was found f r o m the first sampling date, with alates in l o w e r n u m b e r s than apterous adults. The population reached a p e a k at the second sampling with 20.7 + 5.1 individuals per leaf. Alate adults and nymphs increased m o r e than apterous adults. The population d e c l i n e d slowly o v e r the f o l l o w i n g five samplings.

3.2. Population dynamics of M. nicotianae in 1991

tipper

[] Lower (a)

) 1

The population of M. nicotianae in the seedbed remained low (Fig. 1), the highest density being found

t

l

Upper

!

Lower

....

0

.11

21

•_! ~1

10

2e

ao

le

June

20 Jul?'

• Upper [] Lower

~20;

4

)

ii

21 ~4a),

al

la

20 June

aa

le

20 JuLy

Fig. 4. Diseased M. nicotianae on upper and lower halves of tobacco plants in the untreated plot A per sampling date in 1991: (a) mean ( + SE) number per leaf; (b) contribution of diseased aphids to total number; (c) contribution of diseased aphids to the total aphid population.

t

L At

o J_

~ 2A ~ay

31

10

~s ~une

3e

le

20 Ju2~

Fig. 5. Mean (+SE) number of parasitised M. nicotianae per leaf on upper and lower halves of tobacco plants in the untreated plot A per sampling date in 1991.

62

D.P. Lykouressis, G. V, Mentzos /Agriculture, Ecosystemsand Environment 52 (1995) 57-64

on 1 May. Alates were present from the first sampling date as well as apterous adults. Nymphs constituted the largest proportion of the population. In the seedbed no diseased or parasitised aphids were found and only one adult of Coccinella septempunctata (Linnaeus) was observed. In treated plot B, the total population increased after transplanting but after spraying on 31 May it decreased to 1.7_ 0.3 aphids per leaf and then increased again to the end of the season (Fig. 2(e) ). The spray of 12 June had little effect on the aphid population. Aphids appeared from the first sampling date on the upper half of the plants and were present until the end of the sampling period. On the lower half, aphids were absent or in low numbers until 20 June when a small increase was observed (Fig. 2(e) ). Alate adults were found on the upper half of the plants from the first sampling (Fig. 2(d)). Apterous adults and nymphs constituted the largest proportion of the population at each sampling date. Diseased aphids were only found on 10 July on the upper half (0.6%). The number of mummies was small on the lower and almost absent from the upper half of the plants. A few adults and larvae of C. septempunctara as well as larvae of Syrphidae and Chrysopidae were found. Aphid population differences between upper and lower halves were significant only for nymphs and apterae. In the untreated plot A, the population increased sharply after the first two samplings, attaining its peak on June 30 (Fig. 3). Aphid population densities at the various stages followed a similar pattern for both halves of the plants, being much greater on the upper (peak on 30 June, 241.3 + 30.9 per leaf) than on the lower half (peak on 10 July, 36.5 ___6.5 per leaf (Fig. 3(e) ). Alate adults were present from the first sampling until the end of May and increased again from 20 June (Fig. 3(d)). Significant differences were found in the total number of aphids ( F = 392.74, P < 0.0001 with 1 and 672 d.f.), apterous nymphs of the four first instars (F=417.93, P<0.0001 with 1 and 672 d.f), fourth alate instar nymphs ( F = 15.02, P<0.0001 with 1 and 672 d.f.) and apterous adults ( F = 8.27, P < 0.05 with 1 and 672 d.f.) between upper and lower halves of the plants. Diseased aphids were observed on 31 May and attained a maximum on 10 July (Fig. 4). Higher num-

bers of diseased aphids were found on the upper than on the lower half, although the difference was only significant on 10 July (P < 0.01) (Fig. 4(a) ). Parasitised aphids were found from the first sampling and peaked on 10 July. Mummies were found in much lower numbers in the upper than on the lower half (Fig. 5), significant differences between the two halves being found (F=51.98, P<0.0001 with 1 and 672 d.f.) at all dates except for 10 June. A small number of aphid predators was found during the entire sampling period, C. septempunctata in particular. The population fluctuations in plots A and B are shown in Figs. 2 and 3. Significant differences were found in the number of aphids of various instars, diseased and parasitised as well as in various aphid predators between the two plots.

4. Discussion

The analysis of population structure in 1990, revealed that the proportion of alate aphids to the total population was very small on 30 May. A proportion of the total population most probably came from the seedbed at transplanting, as was found in the seedbed in 1991. The population of M.nicotianae was small in 1990 and attained its maximum in early June. In 1991, aphid population densities were much higher and peaked at the end of June. In 1991, alate adults were found in the seedbed from 1 April which implies that M. nicotianae reproduces anholocyclically in this area (cf. Blackman, 1987). Holocyclic reproduction ofM. nicotianae certainly also occurs in Greece (Blackman and Spence, 1992) because fertile winter eggs of M. persicae were found on P. persica from 1977 (D. Lykouressis, unpublished data, 1977). Fusco and Thurston (1968) also reported that M. persicae overwintered anholocyclically on Cruciferae and Chenopodiacceae in the cool areas of Kentucky, USA. With aphids present at all samplings in the seedbed, it seems advisable to spray because no natural enemies were present then. The spray with endosulfan on 31 May drastically decreased the population of M. nicotianae but dramat-

D.P. Lykouressis, G. V. Mentzos /Agriculture, Ecosystems and Environment 52 (1995) 57~4

ically reduced the number of mummies until the last sampling. The second spray reduced the aphid populations but generally had a limited effect and hence could be avoided. Naturally occurring biological control agents were not capable of controlling aphid population densities. Aphidiids and pathogenic fungi were more important than coccinellids, syrphids and chrysopids. Because the rate of diseased aphids was higher on the lower half of the plant, irrigation, which increases the local relative humidity could be used to enhance the spread and germination of the spores of pathogenic fungi. Parasitised aphids tend to move and mummify in places other than the initial feeding site (Van den Bosch et al., 1962; Behrendt, 1968; Powell, 1980; Lykouressis and Van Emden, 1983; Messing, 1986). As a consequence, a considerable number of mummies are removed with the picked leaves, which substantially lowers the rate of parasitisation. Picking the leaves in strips can thus be recommended to reduce this effect. Again, some tobacco plants could be left intact in the field.

5. Conclusions

M. nicotianae is a serious pest of tobacco in Greece. Aphids appear early in the seedbed and it is therefore advisable to spray at this stage when natural enemies are very scarce. Aphidiid parasitoids and fungal diseases were more important mortality factors than the various predators. Because mummies concentrate on lower leaves, agricultural practices that reduce removal of the mummies in picked leaves, such as maintaining a proportion of whole tobacco plants, or picking leaves in strips, or even the use of alternative host plants to increase parasitoid activity, could be of importance. Practices such as a combination of flooding and overhead irrigation, could increase biological control from fungal diseases as a result of higher relative humidity and the spread of spores.

63

Acknowledgements The authors thank Dr R.L. Blackman (Natural History Museum, London) for the identification of M. nicotianae, Professor P. Kaltsikis (Agricultural University of Athens) for assistance in statistical analysis, and V. Mentzos who kindly assigned the tobacco field where this research was conducted.

References Behrendt, K., 1968.Das AbwandernparasitierterAphidenvon ihren Wirtspflanzenund eine Methodezu ihrerErfassung. Beitr.Entomol., 18: 293-298. Blackman, R.L., 1987. Morphologicaldiscriminationof a tobaccofeeding form from Myzuspersicae (Sulzer) (Hemiptera:Aphididae), and a key to New WorldMvzus (Nectarosiphon) species. Bull. Entomol.Res., 77: 713-730. Blackman, R.L. and Spence,J.M., 1992.Electrophoreticdistinction betweenthe peach-potatoaphid,Myzus persicae and the tobacco aphid, M. nicotianae (Homoptera: Aphididae). Bull. Entomol. Res., 82: 161-165. Blackman, R.L.and Takada, H., 1975. A naturallyoccurringchromosomaltranslocationin Mvzus persicae (Sulzer). J. Entomol., 50: 147-156. Chamberlin,F.S., 1958. Historyand status of the green peach aphid as a pest of tobaccoin the UnitedStates. Tech. Bull. 1175,USDA, Washington,DC. Dominick,C.B., 1949. Aphidson flue-curedtobacco.J. Econ. Entomol., 42: 59-62. Eastop, V.F. and van Emden, H.F., 1972. The insect material. In: H.F. van Emden (Editor), Aphid Technology,AcademicPress, London, pp. 1-45. Fusco, R.A. and Thurston,R., 1968. Anholocyclicoverwinteringof the greenpeachaphid in Kentucky.J. Econ.Entomol.,61: 13831386. Harlow, C.D., Southern, P.S. and Lampert, E.P., 1991. Geographic distribution of two color forms, carboxylesterase activity and chromosome configurationof the tobacco aphid (Homoptera: Aphididae) in North Carolina. J. Econ. Entomol., 84: 11751179. Kennedy,J.S., Day, M.F. and Eastop, V.F., 1962. A Conspectus of Aphids as Vectors of PlantViruses. CommonwealthInstituteof Entomology,London, 144 pp. Lampert, E.P., 1989. Seasonal abundanceand within-plantdistributionof aphids (Homoptera:Aphididae)on flue-curedtobacco. J. Econ. Entomol.,82:114-118. Lampert, E.P. and Dennis, C.A., 1987. Life history of two color morphs of the green peach aphid (Homoptera: Aphididae) on flue-curedtobacco. Tob. Sci., 31: 91-93. Lykouressis,D.P., 1991.Ephithrix hirtipennis ( Melsheimer), a new pest of tobacco in Greece, with notes on its morphology,bioecology and control.Entomol.Hellenica,9: 81-85.

64

D.P. Lykouressis, G. V. Mentzos /Agriculture, Ecosystems and Environment 52 (1995) 57--64

Lykouressis, D.P. and Van Emden, H.F., 1983. Movement away from feeding site of the aphid Sitobion avenae (F.) (Hemiptera: Aphididae) when parasitized by Aphelinus abdominalis (Dalman) (Hymenoptera: Aphelinidae). Entomologia Hellenica, 1: 59--63. Messing, R.H., 1986. Biological control of the filbert aphid, Myzocallis co~li, in western Oregon. Ph.D. Thesis, Oregon State University, Corvallis. Mistric, W.J., Jr. and Clark, G.B., 1979. Green peach aphid injury to flue-cured tobacco leaves. Tob. Sci., 23: 23-24. Powell, W., 1980. Toxares deltiger (Haliday) (Hymenoptera: Aphidiidae) parasitizing the cereal aphid Metopolophium dirhodum (Walker) (Hemiptera: Aphididae), in Southern England: a new host: parasitoid record. Bull. Entomol.Res., 70: 407-409. Reed, T.D. and Semtner, P.J., 1991. Influence of temperature on population development of two color morphs of the tobacco aphid (Homoptera: Aphididae) on flue-cured tobacco. J. Entomol. Sci., 26: 33-38.

Semtner, P.J., 1984. Effect of transplantation date on the seasonal abundance of the green peach aphid (Homoptera: Aphididae) and two aphid predators on flue-cured tobacco. J. Econ. Entomol., 77: 324-330. Takada, H., 1986. Genotypic composition and insecticide resistance of Japanese populations of Myzus persicae (Sulzer) (Horn., Aphididae). Z. Angew. Entomol., 102: 43--44. Throne, J.E. and Lampert, E.P., 1985. Age specific honeydew production and life history of green peach aphids (Homoptera: Aphididae) on flue-cured tobacco. Tob. Sci., 29: 149-152. Van den Bosch, R., Schlinger, E.I. and Hagen, K.S., 1962. Initial field observations in California on Trioxyspallidus (Haliday), a recently introduced parasite of the walnut aphid. J. Econ. Entomol., 55: 857-862. Van Emden, H.F., Eastop, V.F., Hughes, R.D. and Way, MJ., 1969. The ecology of Myzus persicae. Ann. Rev. Entomol., 14: 197270.