Experimental and Applied Acarology 33: 203–213, 2004.

# 2004 Kluwer Academic Publishers. Printed in the Netherlands.

Side effects of mancozeb on Typhlodromus pyri(Acari: Phytoseiidae) in vineyards: resultsof multi-year field trials and a laboratory study

PHILIPPE AUGER1,*, SERGE KREITER1, HELENE MATTIODA2

and ANDREA DURIATTI2

1ENSA-M=INRA, Unite d’Ecologie animale et Zoologie agricole, Laboratoire d’Acarologie, 2, Place

Pierre Viala, 34060 Montpellier cedex 01, France; 2DowAgroScience SAS, 6, avenue Charles De Gaulle,

BP 93, 78151 Le Chesnay cedex, France; *Author for correspondence (e-mail: auger@ensam.inra.fr;

phone: þ33-4-99612268; fax: þ33-4-67521554)

Received 20 May 2003; accepted in revised form 22 March 2004

Key words: Laboratory test, Long-term field trial, Mancozeb, Side effect, Typhlodromus pyri

Abstract. The side effects of mancozeb on the predatory mite Typhlodromus pyri were studied in 4-year

field trials on grapevine and in the laboratory. In the field, the effect of mancozeb varied according to

previous mancozeb use. In vineyards where mancozeb had commonly been used over years, this fun-

gicide is generally slightly toxic, in some cases moderately toxic and rarely toxic. In plots were man-

cozeb has never been used, its effect on T. pyri was more pronounced and varied from moderately toxic

to toxic. Despite the toxicity of mancozeb, T. pyri populations have never been eradicated. Laboratory

results obtained with the French CEB guideline no. 167 confirmed those of the 4-year field study:

mancozeb was significantly more toxic to T. pyri populations collected in plots where it had rarely been

used before the field experiment. In plots where mancozeb had been used for a long time, the sus-

ceptibility of T. pyri populations to this fungicide was reduced and female survival, fecundity but also

viability of female progeny were less affected by mancozeb. Even though toxicity of mancozeb increased

in controlled conditions, a significant correlation was established between field and laboratory results.

Introduction

In vineyards, predatory mites of the family Phytoseiidae are important regulators of

spider mite populations. These predators that naturally occur in plants even in

absence of tetranychids are generalist predators (McMurtry and Croft 1997) that

must be preserved using selective plant protection treatments. As a consequence,

the knowledge of the side effects of pesticides on beneficial organisms is important

(Croft 1990). Many studies have shown that the use of the dithiocarbamate fun-

gicide mancozeb in vineyards and in apple orchards reduced the densities of dif-

ferent phytoseiid mite species (e.g., Ioriatti et al. 1992; James and Rayner 1995;

Bostanian et al. 1998). Nevertheless, resistance to dithiocarbamate fungicides of

one species of phytoseiid has been demonstrated (Angeli and Ioriatti 1994) and

tolerance suspected for another species (Vettorello and Girolami 1992).

The aim of our study was to assess the influence of previous mancozeb use (using

mancozeb vs. excluding mancozeb from fungicide programmes) on the toxicity of

mancozeb sprayings to Typhlodromus pyri Scheuten, the dominant species in French

vineyards (Kreiter et al. 2000). A multi-year field trial on different grapevine plots from

different sites was performed to determine whether mancozeb toxicity could be re-

duced, following previous mancozeb use, and to test whether its negative effect on T.

pyri could accumulate over a long period (4 years) leading to outbreaks of tetranychid

mites. The field experiment was completed by a laboratory trial with T. pyri popula-

tions originating from the field experiment to assess their susceptibility to mancozeb.

Material and methods

Field experiment

Trials were conducted in eight plots with various crop protection background located in

various wine-producing regions of France (Bordeaux, Champagne, Burgundy, Rhone

valley and Loire valley). Plots measuring between 2300 and 7800 m2, were in-

vestigated over the 1996–1999 period (1997–1999 for Plot 8). Four of them (Plots 1–4)

were characterised by the common use of mancozeb (5000–15000 g of mancozeb per

hectare per year). In the last four plots (Plots 5–8), this active ingredient had never or

rarely been used before. Treatments were applied by the vine-growers with their own

equipment and according to their own usual pest control practices in terms of product

type and application frequency. Each plot was split into two parts. One was treated with

a mancozeb-based programme (mancozeb subplot). As it was not possible to compare

the mancozeb-treated part with a water-treated subplot (because of commercial vi-

neyards), it was compared to a folpet-treated subplot (used as control plot) because this

active ingredient is known to have no toxic effects on T. pyri (Hassan et al. 1988;

Sentenac et al. 2002). The pesticides used to control other pests (e.g., flufenoxuron,

fenoxycarb) and diseases (e.g., dinocap, quinoxyfen) were neutral for T. pyri (Sentenac

et al. 2002) and no acaricide was used during the 4-year experiment. The density of

phytoseiid mites of each subplot was estimated with five (1996–1997) and nine (1998–

1999) sample units of five vine stocks. The same vine stocks were sampled in the 4

years to assess the potential cumulative effect of mancozeb during the 4-year period.

Twenty leaves were sampled from the middle of shoots of the five vine stocks (four

leaves per vine) of each sample unit throughout the experiment. A total of 100 (1996–

1997) to 180 leaves (1998–1999) per subplot were collected at each sampling date.

Four samples per year were collected: in late spring (end of April–beginning of May),

early summer (June), and summer (beginning of July and end of July–beginning of

August), corresponding to growth stages BBCH 12-15, BBCH 65, BBCH 79 and

BBCH 83 (Lorenz et al. 1994). Following sampling, mites were collected using the

washing method of Boller (1984) and counted under binocular microscope. All the

mites were identified by means of a phase contrast microscope using the key of Chant

and Yoshida-Shaul (1987).

Residual Populations (RP) of T. pyri were calculated and used to compare the

impact of mancozeb treatments. RP corresponded to the ratio between the mean

number of T. pyri in the mancozeb-treated subplot and the mean number of T. pyri

in the folpet-treated subplot.

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Laboratory experiment

Phytoseiids were collected in six plots among the eight of the field experiments.

Three originated from plots where mancozeb was commonly used and the other

from plots where it had never been used before. At the end of the fourth year of the

field experiment, phytoseiid mites of mancozeb-treated and folpet-treated subplots

were collected and reared separately, thus 12 subpopulations were reared and

tested. The effect of the recommended field rate (1400 g a.i.) of Dithane M 451

(80% mancozeb, WP), licensed for the control of downy mildew (Plasmopara

viticola (Berk. and Curt.) Berk. and De Toni), was tested on the 12 subpopulations.

The procedure used to assess the side effects of mancozeb on T. pyri populations

was that of the French CEB guideline no. 167 (Kreiter and Sentenac 1993; Kreiter

et al. 1998). The aim of this method is to evaluate the lethal and sublethal effects of

pesticides on T. pyri. The evaluation is based on the following endpoints: (i) cu-

mulative female mortality 10 days after treatment, (ii) female fecundity during 10

days, (iii) viability of female progeny from day 10 to day 15. Although this method

does not use the most sensitive stage of T. pyri (protonymphs), it provides reliable

results (Sentenac et al. 2002). Testing females allows to get useful data on the

possible detrimental effects of pesticides on female reproduction and on the via-

bility of their progeny. The Global Effect (GE) index (Baillod and Lenfant 1994) is

used to compare the toxicity of pesticides to phytoseiid mites through female

mortality, female fertility and viability of female progeny.

GE %ð Þ ¼ 100 � 100 � M½ �R1R2ð Þ;

where M¼ corrected female mortality as a percentage (Abbott 1925); R1¼fecundity in the treated set=fecundity in the control; R2¼ offspring survival in the

treated set=offspring survival in the control set. Three replicates of 10 females of T.

pyri (young mated females at the beginning of the oviposition period) and glass

support were treated with a solution of mancozeb (0.35 g a.i.=L, on the basis of a

volume application rate of 400 L=ha) using a calibrated Potter spray tower (Potter

1952) (Burkard, Rickmansworth, Hertfordshire, UK) to get a wet deposit of

1.5� 0.1 mg cm�2 (amount arbitrarily chosen in the range given by Baillod and

Lenfant (1994)). Three replicates of 10 females were sprayed with distilled water to

be used as control. Experimental conditions were 21� 1 8C, 65� 10% RH and a

photoperiod of 16:8 (L:D)h. A test is valid when the control mortality rate does not

exceed 15% and when the number of eggs per female per day is higher than 0.8.

Statistical analysis

Statistical analyses of the field experiment data were performed using each plot as a

replicate (one replicate for mancozeb-treated subplot and one replicate for folpet-

treated subplot). As mancozeb is known to have a delayed effect (Zacharda and

Hluchy 1991; Blumel et al. 2000a), densities of T. pyri at the end of the season

(end-summer populations) were analysed to assess the side effects of mancozeb

205

sprayings. The effects (and interactions) of treatment (mancozeb vs. folpet), pre-

vious mancozeb use, year of experiment and plot on phytoseiid mites densities were

analysed with an analysis of variance (mixed model). The same analysis was also

performed with spring populations of T. pyri.

A Student’s t-test (a¼ 5%) was used to analyse the ratios between the RP at the

end of the growing season (end-summer RP) and the RP at the beginning of the

season (spring RP) of the following year obtained in the two types of plots (plots

usually treated with mancozeb before the experiment vs. plots never treated with

mancozeb before the experiment). The quantity of mancozeb applied per hectare

per year during the experiment in plots usually treated with mancozeb and in plots

where mancozeb was not use before the experiment was compared with a Student’s

t-test (a¼ 5%).

A Kruskal–Wallis analysis of variance was performed to compare the densities of

P. ulmi during the 4-year period in mancozeb- and folpet-treated subplots in plots

repeatedly sprayed or not with mancozeb. GE of T. pyri subpopulations obtained in

the laboratory experiment and the effect of mancozeb on the three demographic

parameters (female mortality, fecundity and offspring survival) were analysed with

an analysis of variance completed by the Newman–Keuls test (a¼ 5%). The cor-

relation between RP and GE was estimated to compare field and laboratory results

but not to assess the predictive value of the laboratory experiment.

Results and discussion

Field experiment

Compared to folpet, the detrimental effect of mancozeb on end-summer popula-

tions of T. pyri was significant (F¼ 25.64; p< 0.0023) (Figure 1). Densities of T.

pyri varied with the year of experiment (F¼ 4.99; p< 0.011) but were not influ-

enced by the previous use of mancozeb (F¼ 3.24; p< 0.122) and not by the plot

(F¼ 1.4264; p< 0.255). The phytoseiid mites density was significantly influenced

by interaction between the treatment and the previous mancozeb use (F¼ 8.1;

p< 0.029) and interaction between the year of experiment and plot (F¼ 12.63;

p< 0.0001). Results indicate that there was no significant interaction between the

treatment and the year of experiment (F¼ 2.86; p< 0.066), no interaction between

the treatment and the plot (F¼ 2.27; p< 0.083) and no interaction between the

previous use of mancozeb and the year of experiment (F¼ 1.53; p< 0.24). Second

order interaction was not significant (F¼ 1.33; p< 0.294). According to our results,

the effect of mancozeb sprayings on the density of phytoseiids is less pronounced in

plots where this fungicide was commonly used before the experiment. Detrimental

effect is less frequent and end-summer RP values were on average 2-fold lower in

plots where mancozeb was not used before the experiment (Figure 1).

This difference cannot be attributed to variations in the amount of mancozeb

applied during the experiment because the quantity of active ingredient per hectare

was significantly higher (t¼ 3.01; p< 0.0054) in plots usually treated with

206

mancozeb (10740 g a.i. ha�1 year�1� 750 (SE) vs. 7470 g a.i. ha�1 year�1� 780

(SE)). This result seems paradoxical: the more mancozeb is applied, the less T. pyri

populations are affected by mancozeb whereas according to the literature T. pyri

populations are reduced when the number of mancozeb applications is increased

(Walker et al. 1989; Blumel et al. 2000a). This result becomes consistent if we

hypothesise that a lower susceptibility to mancozeb of T. pyri populations, due to

repeated use of this ingredient, has developed in plots where mancozeb was

commonly used before the experiment. According to field results, Blumel et al.

(2000b) also hypothesised that an increased tolerance towards mancozeb was re-

sponsible for a reduced persistence of its detrimental effects on T. pyri.

Despite quite strong toxicity of mancozeb to end-summer populations (resulting

from sprayings made during the growing season), particularly in plots where it had

not been used previously, mancozeb subplots spring populations of T. pyri of the

following year often recovered to a level comparable to that recorded in folpet

subplots (Figure 2). The effect of mancozeb sprayings was not significant on spring

populations (F¼ 2.27; p< 0.183). In spring, the density of phytoseiid mites was not

influenced by the previous use of mancozeb (F¼ 0.07; p< 0.796) and not by the

experimental plot (F¼ 1.87; p< 0.163). The year of experiment had a significant

effect on the density of T. pyri (F¼ 14.31; p< 0.0007). The density of T. pyri was

significantly influenced by interaction between the treatment and the experimental

plot (F¼ 3.26; p< 0.043) and interaction between the year of experiment and the

plot (F¼ 20.13; p< 0.0001). The effect of treatment was not influenced by the

previous use of mancozeb (F¼ 0.02; p< 0.895) nor by the year of experiment

Figure 1. Densities of T. pyri at the end of the season after repeated mancozeb treatments depending on

previous mancozeb use. Numbers given in parentheses above columns indicate residual populations (RP)

obtained in the different plots (RP¼mean number of T. pyri in the mancozeb-treated subplot=mean

number of T. pyri in the folpet-treated subplot).

207

(F¼ 1.49; p< 0.263) and no interaction between the previous use of mancozeb and

the year of experiment were observed (F¼ 0.145; p< 0.867). As mancozeb ap-

plications ceased on late July–1st week of August, even if mancozeb had a delayed

effect (Zacharda and Hluchy 1991) and mancozeb applications had a significant

effect on T. pyri four weeks after the last treatment (Walker et al. 1989; Blumel et al.

2000a), T. pyri populations could have reproduced and developed with reduced

effect of mancozeb during the time between the beginning of September and winter.

This could reduce differences between population densities of the mancozeb-

treated and folpet-treated subplots and explaining partial or total recovery.

On average, the ratios between spring RP and end-summer RP of the previous

year obtained in plots commonly sprayed with mancozeb were two-fold lower than

in plots never sprayed with mancozeb before the experiment. Nevertheless, due to

quite important variations, population recovery was not significantly different be-

tween the two plant protection practices (t¼�1.55; p< 0.135) (Figure 3). The

consequence of this population recovery could explain that the detrimental effect of

mancozeb was not cumulative year by year, except in 1999 for spring populations

in plots where mancozeb had never been used before. Nevertheless, the same year,

at the end of the growing season, the end-summer RP of the same plots were among

the highest observed during the whole field experiment (Figures 1 and 2).

Panonychus ulmi populations were kept at very low levels during all the field

experiment. This tetranychid mite was only detected in 19% of samples, and when

detected, the average number of mites (adults and juveniles) per leaf was

0.23� 0.11 (SE). Moreover, P. ulmi densities were not significantly higher in

mancozeb-treated subplots than in folpet-treated subplots, regardless the historical

Figure 2. Densities of T. pyri at the beginning of the season following mancozeb treatments applied the

previous year depending on previous mancozeb use. Numbers given in parentheses above columns

indicate the residual populations (RP) obtained in the different plots (RP¼mean number of T. pyri in the

mancozeb-treated subplot=mean number of T. pyri in the folpet-treated subplot).

208

plant protection practices and the year of experiment (H¼ 12.27; p¼ 0.658).

Furthermore, no tetranychid outbreaks were detected the two years following the

end of the field experiment (2000 and 2001).

Laboratory experiment

Mancozeb toxicity to T. pyri was verified and it was more pronounced than in field

trials (Figure 4). On the toxicity scale of Kreiter and Sentenac (1993), mancozeb

toxicity varied from moderately toxic to harmful. The overestimation of toxicity in

a laboratory experiment is common and due to the fact that the experiment is made

to represent a worst case situation (exposure to pesticide, stages of development,

parameters measured). Moreover, Blumel et al. (2000a) have reported that the

effect of mancozeb was less pronounced in the field, even after multiple applica-

tions, than in the laboratory with a single spraying.

Nevertheless, as in the field experiment, mancozeb toxicity was significantly

more pronounced in T. pyri populations which were not usually in contact with this

fungicide (F¼ 10.81; p< 0.0005). This result indicates that T. pyri individuals

collected in plots where mancozeb has been used for a long time developed tol-

erance to this fungicide.

No significant difference was observed between mancozeb-treated subplots and

folpet-treated subplots whatever plant protection practices. Thus, a 4-year period of

mancozeb or folpet application would not be sufficient to detect significant changes

in mancozeb susceptibility of T. pyri populations (loss of tolerance to mancozeb in

folpet-treated subplot from vineyards usually sprayed with mancozeb or loss of

susceptibility to mancozeb in mancozeb-treated subplots from plots in which this

fungicide has never been used before the experiment).

Figure 3. Ratio between spring residual populations (RP) of T. pyri observed in year ‘n’ and autumnal

RP of year ‘n� 1’ following mancozeb treatments applied in year ‘n� 1’ during the 1996–1999 period.

209

Mancozeb significantly affected female mortality (F¼ 5.48; p< 0.0037), po-

tential fecundity (F¼ 6.49; p< 0.0015), and viability of female progeny (F¼ 8;

p< 0.0004) (Figure 5). According to the literature, mancozeb toxicity expression in

phytoseiid mites seems to depend on the species studied: mancozeb was responsible

for high mortality in females of Amblyseius victoriensis (Womersley) but had no

effect on females of Typhlodromus doreenae Schicha (James and Rayner 1995).

Other studies, using different methodologies, showed that mancozeb exhibited no

effect on females of Amblyseius fallacis (Garman) and sometimes caused female

mortality in populations of Amblyseius andersoni Chant but it reduced egg

hatching, female fecundity and affected offspring survival in A. fallacis and A.

andersoni (Ioriatti et al. 1992; Bostanian et al. 1998). According to Baynon and

Penman (1987), mancozeb does not cause significant mortality to adults or im-

matures of T. pyri. At the opposite, Zacharda and Hluchy (1991) have recorded

mortality of T. pyri females ranging from 50 to 90% depending on mancozeb

concentration and Blumel et al. (2000a) have demonstrated that mancozeb reduced

reproduction of T. pyri females. The laboratory method we used allowed us to

demonstrate that this fungicide can affect female survival but also female fecundity

and survival of juveniles in mancozeb-treated females of T. pyri. Once again, these

parameters are more affected in T. pyri populations originating from plots where

mancozeb was not usually used and there was no difference between the two

subplots of each plot. The reduction in susceptibility mainly resulted from a re-

duced toxicity of mancozeb through female mortality (up to half reduced) and

female fecundity (almost two-fold higher) in populations usually in contact with

this fungicide compared to populations never in contact with this active ingredient.

A moderate but significant correlation (r2¼ 0.42; p¼ 0.004) was found between

average end-summer RP and GE replicates of each population. The quite low

Figure 4. Global effect (GE) of mancozeb on various populations of T. pyri when applied at 1400 g a.i.=ha

in the laboratory study depending on previous mancozeb use (means sharing a common letter are not

significantly different (p> 0.05), Newman–Keuls test).

210

coefficient of correlation could be due to many reasons such as: approximations in

T. pyri RP estimations in the field experiment; differences in amount of active

ingredient sprayed between the plots, quality of spraying and volume per hectare

were also variable (vine growers using their own material) resulting in variations in

mancozeb exposure during the field experiment; alternatively, in the laboratory

experiment, phytoseiids were exposed to a constant amount of mancozeb; varia-

tions in GE estimation could also lead to moderate correlation between field and

laboratory results because GE value is given with a confidence interval equivalent

to 17.5% (Bonafos et al. 1999).

It can be concluded that if mancozeb is considered for integrated pest control

programmes in plots where it has been used for a long time and where T. pyri is

present, its use should be minimised in plots where it has never or rarely been used.

A survey indicating the frequency of mancozeb resistant phytoseiid mites

throughout French wine producing regions would be of great interest.

Acknowledgements

We are grateful to M. Patrick Lecigne who initiated and was in charge of the field

studies. M. Jean Valera and the students Raphael Voegelsperger, Jannick Ducarme,

Francois Dal and Julie Perdereau are also deeply acknowledged. We thank

Figure 5. Effect of mancozeb on female mortality, fecundity and viability of progeny of T. pyri

populations when applied at 1400 g a.i.=ha in the laboratory study depending on previous mancozeb use

(means sharing a common letter are not significantly different (p> 0.05), Newman–Keuls test).

211

M. Romain Bonafos for reviewing an early version of the manuscript and Mrs

Annik Lacombe for revising the english version.

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