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Organic Farming The Use of Copper Pesticides in Germany and the Search for Minimization and Replacement Strategies

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Copper pesticides used to control fungal and bacterial diseases such as grapes downy mildew (Plasmopara viticola), downy mildew of hops (Pseudoperonospora humili), apple scab (Venturia spp.), fireblight (Erwinia amylovora) and potato late blight (Phytophthora infestans), play an important role in plant protection. In a 2013 survey of copper application in Germany we found, that while the amounts of copper used per hectare in conventional grape (0.8 kg ha −1), hop (1.7 kg ha −1) and potato-farming (0.8 kg ha −1) were well below those used in organic farming (2.3, 2.6 and 1.4 kg ha −1 , respectively), they were nearly identical to those used in apple growing (1.4 kg ha −1). Due to the smaller farming area, only 24% (26.5 tonnes) of the total amount of copper was applied in organic farming compared to 76% (84.8 tonnes) in conventional farming. Since 2001, the Federal Agency for Agriculture and Food (BLE) promoted a copper research and minimization strategy which was funded with a total of C10.2 million. Our status quo analysis of research in this field shows that some progress is being made concerning alternative compounds, resistant varieties and decision support systems. However, it also shows that new approaches are not yet able to replace copper pesticides completely, especially in organic farming. In integrated pest management, copper preparations are important for the necessary active substance rotation and successful resistance management. The availability of such products is often essential for organic grapes, hops and fruit production and for extending the organic farming of these crops. We conclude that the complete elimination of copper pesticides is not yet practicable in organic farming as the production of several organic crops would become unprofitable and may lead to organic farmers reverting to conventional production. Several existing copper reduction strategies were, however, identified, and some, like modified forecast models adapted to organic farming, varieties more resistant to fungal diseases and new alternative products, already contribute to copper minimization in German agriculture.
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Organic Farming |2017 |Volume 3 |Issue 1 |Pages 66–75
DOI: 10.12924/of2017.03010066
ISSN: 2297–6485
Organic
Farming
Research Article
The Use of Copper Pesticides in Germany and the Search for
Minimization and Replacement Strategies
Stefan K¨
uhne1,*, Dietmar Roßberg1, Peter R¨
ohrig2, Friedhelm von Mering2, Florian Weihrauch3, Sonja Kanthak4,
Jutta Kienzle5, Wolfgang Patzwahl6, Eckhardt Reiners7, Julia Gitzel1
1Julius K¨
uhn-Institut (JKI), Federal Research Centre for Cultivated Plants, Kleinmachnow, Germany
2Bund ¨
Okologische Lebensmittelwirtschaft e.V. (B ¨
OLW), Berlin, Germany
3Bayerische Landesanstalt f¨
ur Landwirtschaft (LfL), Institut f ¨
ur Pflanzenbau und Pflanzenz¨
uchtung (IPZ),
Hopfenforschungszentrum , Wolnzach, Germany
4Bundesverband ¨
Okologischer Weinbau, ECOVIN, Oppenheim, Germany
5F¨
ordergemeinschaft ¨
Okologischer Obstbau e.V. (F ¨
OKO), Weinsberg, Germany
6Naturland Fachberatung Wein- und Obstbau, Sulzfeld am Main, Germany
7Bioland Bundesverband, Mainz, Germany
* Corresponding author: E-Mail: stefan.kuehne@julius-kuehn.de; Tel.: Tel.: +49 3320348307; Fax: +49 3320348425
Submitted: 4 October 2016 |In revised form: 16 October 2017 |Accepted: 30 October 2017 |
Published: 21 December 2017
Abstract:
Copper pesticides used to control fungal and bacterial diseases such as grapes downy mildew
(Plasmopara viticola), downy mildew of hops (Pseudoperonospora humili), apple scab (Venturia spp.),
fireblight (Erwinia amylovora) and potato late blight (Phytophthora infestans), play an important role in
plant protection. In a 2013 survey of copper application in Germany we found, that while the amounts
of copper used per hectare in conventional grape (0.8 kg ha
1
), hop (1.7 kg ha
1
) and potato-farming
(0.8 kg ha
1
) were well below those used in organic farming (2.3, 2.6 and 1.4 kg ha
1
, respectively),
they were nearly identical to those used in apple growing (1.4 kg ha
1
). Due to the smaller farming area,
only 24% (26.5 tonnes) of the total amount of copper was applied in organic farming compared to 76%
(84.8 tonnes) in conventional farming. Since 2001, the Federal Agency for Agriculture and Food (BLE)
promoted a copper research and minimization strategy which was funded with a total of
C
10.2 million.
Our status quo analysis of research in this field shows that some progress is being made concerning
alternative compounds, resistant varieties and decision support systems. However, it also shows that new
approaches are not yet able to replace copper pesticides completely, especially in organic farming. In
integrated pest management, copper preparations are important for the necessary active substance rotation
and successful resistance management. The availability of such products is often essential for organic
grapes, hops and fruit production and for extending the organic farming of these crops. We conclude that
the complete elimination of copper pesticides is not yet practicable in organic farming as the production of
several organic crops would become unprofitable and may lead to organic farmers reverting to conventional
production. Several existing copper reduction strategies were, however, identified, and some, like modified
forecast models adapted to organic farming, varieties more resistant to fungal diseases and new alternative
products, already contribute to copper minimization in German agriculture.
© 2017 by the authors; licensee Librello, Switzerland. This open access article was published
under a Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/).
librello
Keywords: application rate; copper; research program; sales volumes
1. Introduction
Copper pesticides have been used in Germany for al-
most 150 years, controlling plant diseases such as
downy mildew of grapes (Plasmopara viticola) and
hops (Pseudoperonospora humuli), apple scab (Ven-
turia spp.), fire blight (Erwinia amylovora) and potato
blight (Phytophthora infestans). This makes them some
of the oldest plant protection products (PPPs) relevant
today. Until well into the last century, application rates of
20 to 30 kilograms per hectare per year (
kg ha1yr1
),
and occasionally even 80 or more kg ha
1
yr
1
, of cop-
per pesticides were used in conventional farming in
Germany [1].
Soil persistence and the effects on soil organisms are
discussed, nationally and internationally, as possible im-
pacts from years of copper pesticide use. Strumpf et al.
[
2
,
3
] conducted extensive surveys on copper pollution of
soils in organic and conventional grapes, hops and tree
fruit-growing in Germany. They later performed a risk
assessment of soil copper levels based on bioavailable
copper instead of total copper, the previous standard [
4
].
Research has shown that less than 10% of the total copper
in soil is easily mobilized [
5
], and that not only the total
copper content, but also the texture [% sand content] and
pH of the soil, are significant factors influencing copper
mobilization.
The European Commission extended its approval for
the use of copper compounds as fungicides/bactericides
until January 31, 2018. However, this was done on the
condition that appropriate measures are taken to reduce
usage. In as early as 2009, Germany and some other
EU Member States already passed resolutions to sub-
stantially reduce the maximum limits permitted for pure
copper pesticides. Instead of the 6 kg ha
1
year limit
permitted by EU regulations, Germany has a limit of 3
kg ha
1
yr
1
and 4 kg ha
1
year in hops. Under the
aegis of the German Federation of the Organic Food In-
dustry (B
¨
OLW), German organic farming and integrated
pest management associations, in coordination with the
competent authorities, developed a targeted copper min-
imization strategy that aims to reduce the annual net
amount of copper used in crop protection per hectare
and year, even further [6].
This article provides a review of the use of copper
pesticides in crop protection in Germany since 2010 by
crop and farming method (conventional or organic). Pre-
vious studies on the reduction of the use of copper as
a pesticide in Germany are also examined. The tested
strategies are analyzed in terms of their efficacy and suc-
cess, and limitations of the previous copper reduction
strategies are elucidated.
2. Materials and Methods
2.1. Status Quo Analysis of the Use of Copper Pesticides
in German Agriculture and Horticulture
Article 64 of the German Plant Protection Act requires
that manufacturers, distributors and importers of plant
protection products report to the BVL (Federal Office of
Consumer Protection and Food Safety) with their annual
domestic sales of such products and the active substances
contained in them by amount. The BVL kindly provided
the statistics on the sales of copper pesticides in Germany
from 2010 to 2014.
Julius K
¨
uhn Institute (JKI) has regularly conducted sur-
veys on the use of chemical plant protection products in the
main agricultural and horticultural crops in Germany since
2000. They have been continued as “PAPA surveys”, cate-
gorized under a different legislative framework since 2011
[
7
]. PAPA is an acronym for Panel Pesticide Applications.
Networks of crop-specific survey farms that gather and re-
port detailed annual data on pesticide use were established
under the PAPA program. The selected crops (winter wheat,
winter barley, winter rye, corn, potatoes, sugar beet, dessert
apples, hops and grapes) are those considered most rel-
evant for the National Action Plan on Sustainable Use of
pesticides [
8
]. Data on the use of copper pesticides can
also be gathered from these surveys. It should be noted
that the PAPA surveys only collect data from conventional
farms; German organic farming associations collect the cor-
responding data on organic farming. This is a component
of the JKI’s copper pesticide reduction strategy paper with
specific consideration of organic farming [6].
2.2. Assessment of the Status Quo of Research on the
Minimization and Replacement of Copper Pesticides
in Germany
Since 2001, the Federal Program for Organic Farming
and Other Forms of Sustainable Agriculture (B
¨
OLN) has
funded research projects aiming to contribute to the re-
duction of copper used in plant protection. The results
and resource needs of these projects are summarized
below. These measures were supported by the Euro-
pean CO-FREE Project (Innovative strategies for copper-
free, low-input and organic farming systems, 2012-2016;
funding budget: 3 million euros), in which eleven Eu-
ropean partners collaborated to find alternatives to cop-
per. The results of the CO-FREE project were not in-
cluded in this analysis because the final reports were not
yet available. The individual projects funded by B
¨
OLN
were examined prior to our literature search. Relevant
projects were filter-searched on the Federal Program web-
67
site (https://www.bundesprogramm.de/index.php?id=916,
Accessed on 14 September 2016). A total of 67 projects
involving research on copper reduction were identified using
the keyword “copper” to search the list of “Research and
Development Projects” under the heading “Crop”. A com-
parative analysis of these projects was then performed (e.g.
aim of the projects, effective ingredients, efficacy, costs).
3. Results
3.1. Status Quo of the Use of Copper Pesticides in
German Agriculture and Horticulture
The estimated amounts [kg ha
1
] of copper used in con-
ventional farming in Germany in 2003 are shown in
Table 1
.
The amounts used for conventional farming of potatoes,
hops and grapes were significantly lower than those used
in organic farming. The copper application rates were less
than 1 kg ha
1
yr
1
in potato and grape-growing, and ap-
proximately 1.7 kg ha
1
yr
1
in hop-growing. Conversely,
the amounts of copper used for apple-growing were almost
equal in organic farming (average of 1.41 kg ha
1
yr
1
in 2010 to 2013) and conventional farming (1.4 kg ha
1
yr
1
in 2013). However, comparison of the total amounts
of copper used in both farming systems (Tables 1 and 2)
showed that, when adjusted for differences in the sizes of
application areas, only 24% (26.5 metric ton, t) of the total
amount of copper was used in organic farming compared
to 76% (84.8 t) in conventional farming.
Table 1.
Estimated amounts of copper used [pure copper
in kg ha
1
] in conventional farming in Germany in 2013
relative to the application area.
Potatoes Apple Grapes Hops Total
Application area 2,500
25,500 36,800 10,400 75,200
[ha]
Copper spray rate 0.8 1.4 0.8 1.7 -
[kg ha1]
Pure copper total 2 35.7 29.4 17.7 84.8
[t]
Table 2.
Estimated amounts of copper used [pure copper
in kg ha
1
] in organic farming in Germany in 2013 relative
to the application area.
Potatoes Apple Grapes Hops Vege- Total
tables
Application 3,500
2,100
7,700 84 400
13,784
area [ha]
Copper spray 1.38 1.5 2.29 2.6 2 -
rate [kg ha1]
Pure copper 4.8 3.1 17.6 0.2 0.8 26.5
total [t]
Table 4 lists only those crops in which copper pesticides
were used in integrated pest management. They were not
used in any arable crops except potato. Table 4 clearly
demonstrates how copper oxychloride (trade name: Fungu-
ran), which was initially the most prevalent active ingredient,
was replaced by copper hydroxide (trade names: Cuprozin
Liquid, Cuprozin Progress, Funguran Progress, and Kocide
OPTI) over the analyzed time period. The applied quantities
of copper oxychloride decreased from 163.7 t in 2011 to
1.8 t in 2014 (Table 5). The reverse was observed for cop-
per hydroxide. The application rate of this active substance
increased approximately three-fold, from 45.6 t (2011) to
132.6 t (2014). Use of the other two copper- containing
active ingredients (copper sulfate and copper octanoate)
was marginal. Because basic copper sulfate (trade name:
Cuproxat) is only allowed in grape- growing and does not
play a significant role, at least in conventional agriculture,
it was not included in the table. Copper octanoate (trade
name: Cueva) is allowed in potatoes, apples, grapes and
ornamental plants, but is only used in viticulture in conven-
tional farming.
In organic farming, the application of copper-containing
pesticides is based on forecast model predictions and not
always on the total cultivated area (except in hop- grow-
ing). This comprises over 90% of the total organic farming
area. Table 3 shows the amounts of copper used in organic
viticulture in recent years. The differences in copper ap-
plication rates between the different growing regions are
sometimes substantial. This can be attributed to regional
differences in climatic conditions and weather profiles be-
tween the different growing regions. A regional analysis was
performed on part of the collected data (Figure 1). Compar-
ison showed that the lowest amounts of copper are used in
the Ahr grape-growing region [9].
Table 3.
Average copper application rates [pure copper kg
ha
1
] in organic grape-growing in 2010 to 2013 based on the
size of the treated vine area. Copper pesticides were only
applied to approximately 90% of the total cultivated area.
Grapes 2010 2011 2012 2013
Total area [ha] 5,200 6,900 7,400 7,800
Analyzed area [ha] 1,894 2,260 2,408 2,868
Copper application rate 2.23 1.98 2.34 2.29
[kg ha1]
The highest amounts of copper were used in organic
hop-growing due to the high amount of foliage per unit
area. Application rates in hops exceeded 3 kg ha
1
yr
1
in
four out of six years (Table 6). The small scale of organic
cultivation of this crop (max.85 ha in 2015) should be noted.
68
Figure 1.
Average copper application rates [pure copper kg ha
1
] in organic viticulture by growing region in Germany
from 2010 to 2013.
Table 4. Size of the area treated with copper-containing active substances in conventional farming [% cultivated land]
Active Copper oxychloride Copper hydroxide Copper
substance octanoate
Year Apple Wine Hops Potato Apple Wine Hops Wine
2011 61.6 16.7 77.0 1.8 37.4 21.9 0.0 1.0
2012 51.0 21.3 42.3 0.0 44.4 28.9 28.9 1.1
2013 32.3 9.8 18.6 7.0 67.1 39.0 35.5 1.1
2014 2.9 0.0 0.0 2.6 90.8 48.1 68.2 0.2
Table 5.
Estimated crop-specific amounts [t] of copper-containing active substances used in conventional farming from
2011 to 2014.
Year Copper oxychloride Copper hydroxide Copper Total
octanoate
Year Apple Wine Hops Potato Apple Wine Hops Wine
2011 57.0 35.0 71.7 0.4 35.9 9.3 1.6 210.9
2012 45.7 50.3 33.5 36.9 20.4 8.5 1.1 196.4
2013 25.1 15.8 13.6 1.2 42.1 36.0 10.6 1.1 145.5
2014 1.8 n.s. n.s. 2.9 52.8 48.9 28.0 0.1 134.5
n.s.: not specified
69
Table 6.
Average copper application rates [pure copper
kg ha
1
] in organic hop-growing in 2010 to 2015. Copper
pesticides were applied to 100% of the hops area.
Hops 2010 2011 2012 2013 2014 2015
Total area 76 81 84 84 80 85
[ha]
Copper
application
rate [kg
ha1]
3.9 3.7 3.6 2.6 3.3 1.5
The copper application rates in organic fruit-growing on
the other hand, were less than 2 kg ha
1
yr
1
. A general
decrease in the amount of copper used in apples, peaches,
pears and stone fruit occurred over the observation period
(Table 7).
Regarding potatoes, farms associated with Demeter As-
sociation do not use copper in potato and vegetable-growing
and sometimes accept the risk of considerable yield losses,
alternatively they switch to low-infestation regions to protect
critical crops [
10
]. The copper application rates in organic
potato-growing were below 2 kg ha1yr1(Table 8).
In organic vegetable-growing, a substantial percentage of
farming area is managed in accordance with the minimum
limits of the EU organic farming regulations alone, and the
German farming associations have not yet recorded the cop-
per application rates there. The average copper application
rates reported in Table 9 are, therefore, based on reports from
only two organic farming associations, Bioland and Naturland.
Pumpkin was the sole crop in which copper products were
used in all four years studied. In cucumber, fennel, leek and
ornamentals, copper was used in only one out of 4 years.
3.2. Projects Funded with Public Funds (Federal Organic
Farming Scheme and Other Forms of Sustainable
Agriculture – B ¨
OLN)
Since its establishment in 2001 to 2015, B
¨
OLN has funded
a total of 67 projects for research on copper replacement
and minimization. The B
¨
OLN Federal Organic Farming
Scheme has awarded a total of 10.2 million euros in grants
(Table 10).
Table 7.
Average copper application rates [pure copper
kg ha1] in organic fruit-growing in 2010 to 2013.
2010 2011 2012 2013
Total area [ha] 3400 3700 3900 3900
Apple 1.59 1.3 1.31 1.47
Pear 1.49 1.1 1.26 1.07
Peach 2.21 1.9 2.0 1.7
Stone fruit 1.28 0.94 0.99 0.83
Table 8.
Average copper application rates [kg ha
1
] in or-
ganic potato-growing in 2010 to 2013 based on the size of
the application area. Copper pesticides were applied to only
about 40 to 50% of the cultivated area in organic farming.
Demeter Association member farms are not permitted to
use copper products.
Potatoes 2010 2011 2012 2013
Total area [ha] 8200 8300 8000 8100
Copper application rate [kg ha1]1.36 1.60 1.87 1.38
on treated areas
Table 9.
Average copper application rates [pure copper kg
ha1] in organic vegetable-growing in 2010 to 2013 based
on the size of the application area. Copper products are
used in only about 2 to 4% of the total cultivated area of the
Bioland and Naturland farms.
Crop 2010 2011 2012 2013
Total area [ha] 10,590 10,890 10,470 10,470
Celery 2.32 1.1 0.85 -
Pumpkin 1.80 2.1 1.4 0.36
Cucumber 1.43 - - -
Fennel - 0.9 - -
Leek - 3.0 - -
Asparagus - 2.0 1.2 1.09
Greenhouse crops - 1.4 1.3 -
Ornamental crops - - 0.1 -
Other vegetables* - 1.8 1.1 -
* Outdoor vegetable crops produced on small scale
The number of projects supported varies by crop type,
in some cases greatly. Most of the projects carried out in-
volved crops that are highly dependent on the use of copper,
e.g., fruit and grapes. Although relatively large amounts of
copper pesticide are regularly used in hop-growing, only
two projects funded so far involved this crop. Projects that
were not unique to a given crop type or which contributed
to the minimization of copper indirectly were included in the
subcategory “Others”.
3.2.1. Number of Alternative Products Tested and Their
Effects in the Field
At least 278 alternative products were field-tested alone or
combined (Figure 2). At least 56 and 182 of these were
tested in the crops “grapes” and “fruit”, respectively. In other
crops, a smaller number of projects and a larger number of
variety and field tests were conducted.
At least 90 of the tested products showed a significant
effect on the comparison variant in these trials. In some
cases, however, data was from only one-year trials, thus
requiring further investigation.
70
Table 10.
Amount of funding from the “Federal Organic Farming Scheme and other forms of sustainable agriculture”
(B
¨
OLN) for research on the minimization and replacement of copper pesticides in Germany (from 2001 to 2015) by crop
type.
Project Status Grapes Fruit Vegetables Hops Potatoes Others Total
Finished 11 12 10 2 8 6 48
Ongoing 3 14 - - - 1 18
Total 14 26 10 2 8 7 67
Public funds in C1000 2,394 2,937 1,923 255 1,593 1,122 10,225
Figure 2.
Number of copper alternative/replacement products field-tested under the B
¨
OLN program and their effects in
different crops. Symbols: ++ (significant effect), + (effective in the laboratory/greenhouse but not in the field), 0 (no effect).
In most cases, the copper alternatives were first tested
in the laboratory and/or greenhouse (especially in fruit-
growing) prior to field testing. They were only tested in
the field if they showed good efficacy in the indoor setting.
However, some substances were employed based on practi-
cal experience or data from literature. Consequently, some
of the products demonstrated efficacy only under certain
conditions, e.g., very good effects in the laboratory or good
effects in the greenhouse but not in the field. A lack of rain
resistance or UV resistance was frequently the presumed
reason for these discrepancies. This was the case for 21
products.
At least 106 of the tested products showed no effect
in the field. At least 61 of these alternative products had
been tested in fruit-growing. No data could be collected on
85 products for various reasons; for example, in one case,
a product was to be tested on fungal diseases, which did
not develop during the observation period. In other cases,
the trials have not yet been completed, so no conclusions
regarding the efficacy of the products can be made.
3.2.2.
Copper products tested at reduced application rates
In addition to alternative substances, 139 copper compounds
were tested under field conditions in reduced application
rates, new formulations or combinations (Figure 3).
Potato was the crop on which most (n = 60) of these cop-
per compounds were tested. Improved spray technology
and forecasting models were developed in these projects.
In total, 21 and 38 products, respectively, were tested in the
crops “grapes” and “fruit”.
105 field trials showed significant effects of products
tested at reduced copper application rates (Figure 3), in-
cluding all products tested in hops, grapes and vegetable-
71
growing. Only two products tested in fruit-growing showed
no effect. Problems such as difficulty producing a homoge-
neous spray mixture or clogging of the spray nozzles also
led to the failure of sprayed products.
3.2.3. Other Project Funding
As well as finding alternative products to replace copper,
other elements of plant protection were investigated, e.g., the
development of more resistant crop varieties, better spraying
techniques, and improved forecasting models (Table 11).
Brief descriptions of the projects by crop are pre-
sented below.
Potato:
Several projects were funded in potato-growing:
Two dealt with development and implementation of the ECO
SIMPHYT forecast model, which contributes directly to cop-
per minimization because it can, among other things, give
farmers precise spraying date recommendations. Another
two projects dealt with the use of preventative measures
to control late blight (P. infestans) so that less copper can
be applied. Two more projects investigated new resistant
varieties and one, an improved spraying technique (lower
leaf spraying) which may contribute to reducing the copper
application rate.
Grapes:
In contrast to potato-growing, the breeding of
resistant varieties was a main focus of research in viticul-
ture (Table 11). A total of five projects were funded. Two
projects investigated the resistance of old grape varieties or
the combination of different fungus-resistant grape varieties
(PIWI), among other things. Three projects were performed
for additional research into the biology of grapevine downy
mildew (Plasmopara viticola). A reduced copper application
rate of 2 kg ha
1
yr
1
is sufficient when Peronospora in-
festation levels are low. The efficacy of algae extracts and
clays can be quite satisfactory under these conditions.
Fruit:
Projects in fruit-growing involved research on fall
foliage reduction [
11
14
]. This is important because over
winter, leaves with apple scab fall and re-infect trees in
spring. As in viticulture, research into the biology of various
pathogens (mainly apple scab) in fruit-growing was also
funded [
15
]. All the results from these trials aim to feed into
forecasting models and software for application intensity
and risk assessment of copper pesticides used by farmers
[
16
,
17
]. Variety trials and two improved spraying technique
trials were also conducted [18].
Vegetables:
Variety selection trials were performed and
cultivation methods were tested in all six projects performed
in vegetable-growing. Hot water treatment of seeds suc-
cessfully reduced carrot leaf blight (Alternaria dauci) in one
study [
19
]. Moreover, a promising licorice-based product
(Glycyrrhiza glabra) was developed to control fungal dis-
eases in cucumber, tomato and potatoes [20].
Hops: The research projects performed in hops tested
the ability of alternatives to copper and sulfur-containing
pesticides as well as copper combinations to reduce the
copper application rate. Unfortunately, none of the investi-
gated products satisfied the requirements.
Inability to satisfactorily control primary infection of hop
downy mildew (Pseudoperonospora humuli) was the fun-
damental problem. Preventive application was only able to
prevent secondary infection. The use of quassia to control
the hop aphid achieved reasonable results [21].
Table 11. Strategies for reducing copper application assessed within German research projects since 2001.
Strategies Number of Projects
Grapes Hops Fruit Vegetables Potatoes Others Total
Alternative compounds 5 1 7 (+4*) 4 1 2 20 (+4)
Varieties 5 - 1 6 2 - 14
Decision support systems - - 4 - 2 - 6
Pest biology 3 - 2 - - - 5
Application technique - - 2 - 1 - 3
Others: Communication, prevention (e.g., fall foliage) - - 5 - 2 3 10
* Ended in 12/2016
72
Figure 3.
Number of copper products field-tested under the B
¨
OLN program and their effects in different crops. Symbols:
++ (significant effect), + (effective in the laboratory/greenhouse but not in the field), 0 (no effect).
4. Discussion
4.1. Use of Copper Pesticides in Integrated Pest
Management
The use of copper-containing pesticides in German grapes
and hop growing is focused on the last application of the year
(in August) in order to control downy mildew of grapes and
hops. This application, therefore, has an important key func-
tion in terms of the necessary active ingredient rotation and
successful resistance management. It should be noted that
the copper application rates used for the final treatment in inte-
grated viticulture are substantially higher than those normally
used in organic viticulture. To date, no cases of resistance to
copper-containing pesticides have been reported- since the
first use of copper-containing substances in plant protection
about 150 years ago. This underscores the importance of
copper pesticides for crop protection as, until now, no other
plant protection product has shown such a long duration of ef-
fect. In fruit-growing, copper pesticides are mainly used in the
winter months (December to March) to control apple canker
(Nectria galligena), and in March to control bark scab. The
current use of copper-containing pesticides in conventional
potato-growing is negligible.
5. Use of Copper Pesticides in Organic Farming
The collaboration between organic farms, researchers and
medium-sized pesticide companies to promote copper re-
duction in recent years has led to further reduction of the
amounts of copper used in various crops. Key factors that
have contributed to successful copper reduction include the
development of forecasting models that accurately deter-
mine the need for and timing of pesticide application [
22
],
the implementation of agronomic and technical measures
[
11
] and the selection of less susceptible varieties [
23
]. The
use of alternative natural pesticides and plant strengtheners
[
20
,
24
] must be incorporated in an overall strategy. Then,
less effective products may also be useful components of
copper minimization under certain conditions (e.g., weather,
timing of application). Despite these advances, it is still
neither possible nor advisable to completely refrain from
using copper pesticides in organic farming.
Organic viticulture and hop-growing are particularly
dependent on the availability of copper pesticides. After
failure to get potassium phosphonate included in Annex II
of Regulation 889/2008, no effective alternative products
for these crops appear to be on the horizon any time
soon. Furthermore,the willingness of conventional grape
growers to change to organic farming depends largely on
the availability of options for effective control of downy
mildew of grapes (Plasmopara viticola) and grape black
rot (Guignardia bidwellii ).
In organic hops production, the application rates of cop-
per pesticides used to reduce hop downy mildew (Pseu-
doperonospora humuli) can even be reduced to less than
3 kg ha
1
yr
1
(pure copper) during years of low disease
pressure. However, rates of up to 4 kg ha
1
yr
1
may still
73
be needed in years with high disease pressure, meaning
that a high flexibility of copper application is necessary in
this crop [
25
]. If copper-containing pesticides were banned,
it is feared that organic hop farms would go out of business
because equivalent alternatives are still lacking [25].
Regarding the control of apple scab (Venturia inae-
qualis) in organic orchards, improvements have already
been developed and tested in the context of copper mini-
mization strategy in the following areas: cultivation methods
[
12
], fall foliage management [
13
], the use of resistant vari-
eties [
15
], and the possible use of alternative products [
14
].
The search for new products for organic fruit production
is focused on modular strategies designed to ensure that
copper use is reduced while achieving the same or even
better plant health [12].
Potato late blight (Phytophthora infestans) can cause
severe economic losses in organic potato production [
25
].
In times of high infestation pressure and adverse weather
conditions, the reliability of effect of the alternative prod-
ucts tested so far is still too low for them to be equivalent
substitutes for copper-containing pesticides [
26
]. Fore-
casting models for late blight were adjusted to the condi-
tions of organic farming and to the comparatively lower
nutrient levels in the soil. This led to a reduction of copper
applications [
21
,
27
]. Wilbois et al. [
28
] predict that the
trend towards copper reduction will continue in the future,
and that the level of copper application reached in about
10 to 15 years will correspond to the natural uptake of
copper as a plant nutrient.
In vegetable-growing, copper pesticides are only rel-
evant in a few crops and are usually applied at rates of
less than 2 kg ha
1
yr
1
. The control of downy mildew
in lettuce and cucumber is a major focus. Resistant vari-
eties [
29
] and new licorice preparations were successfully
tested [
19
,
30
,
31
]. Effective alternative pesticides for these
applications can be expected in the future.
5.1. Research Funding to Promote Copper Reduction in
Crop Protection
Research funding to promote copper reduction in German
agriculture has focused on the following fields of study:
Further development of forecast models
Development of resistant varieties
Improved spraying techniques
Improved cultivation techniques
Introduction of new copper products with low copper
concentrations
Development and introduction of copper-free alterna-
tives
Implementation and optimization of overall plant pro-
tection strategies
Improvement of copper pesticide impact assessment
Our status quo analysis clearly showed that German re-
search on copper reduction and replacement is based on
close collaboration between research, practice, advisory
services and industry, and needs to be continued and fur-
ther developed.
At present, it is still not possible to completely refrain
from using copper pesticides in organic farming. Emerging
diseases, such as grape black rot (Guignardia bidwellii), can
result in partial to complete yield loss [
32
]. The combination
of copper- containing pesticides with sulfur-based products
is currently the only effective way to combat grape black rot
in organic viticulture [
32
]. It should be noted that research
funding in Germany is accompanied by other measures
that contribute to successful copper minimization. This
includes the advancement of Strategy Paper on Copper Re-
duction in Plant Protection [
6
] and the annual conferences
on the theme of “Copper as a Pesticide”, which are jointly
organized by the German Federation of the Organic Food
Industry (B
¨
OLW) and the Julius K
¨
uhn Institute. These are
important contributions to continuously documenting the
progress made, and measures needed, to achieve copper
reduction.
6. Acknowledgements
Many thanks to Hubert Ostbomke of the Federal Agency
for Agriculture and Food (BLE) for providing the data and
information about research projects. Thanks also to Hella
Kehlenbeck from the JKI Institute for Strategies and Tech-
nology Assessment for research information.
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... There is a substantial difference between the maximum quantity of copper permitted for a specific use (crop/disease) and its real use, as already highlighted in Switzerland, France, and Germany [18][19][20]. For example, a survey in Switzerland found that organic farmers use, on average, between 3 and 80% of the maximal permitted amount of copper depending on the crop, indicating a high awareness among farmers of the need to reduce copper use [18]. ...
... Even though various tools and strategies to reduce copper-based plant-protection products, such as resistant varieties, cultural measures, decision-support systems, and alternative plant-protection products, are available for farmers [22], completely abandoning copper fungicides would lead to high yield losses in many crops at the current time [19]. To develop strategies and pathways for a complete phasing out of copper-based plantprotection products, policymakers need information on the current dependency on copperbased plant-protection products, the implementation of alternative strategies, and the need for copper alternatives in European organic-crop production. ...
... The present study aimed at filling this data gap by combining an expert survey on use of copper in individual crops with land-use data in 12 European countries, and therefore covering 84% of the European horticultural area. Other studies assessing copper use in organic agriculture have either focused on certain regions (e.g., Switzerland [18] or Germany [19]) or on specific crops (e.g., olives, citrus, tomatoes, and potatoes [21]). The present survey takes into account reductions of copper limits (from 6 kg ha −1 y −1 to 28 kg ha −1 in 7 years) after 2018 as a result of regulation (EU)2018/1981 [15], while other surveys which were conducted before 2018 [18,19,21] use the limits in force at that time, which has to be taken into account when comparing results. ...
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... There is a substantial difference between the maximum quantity of copper permitted for a specific use (crop/disease) and its real use, as already highlighted in Switzerland, France and Germany (Speiser et al., 2015, Kühne et al., 2017, Andrivon & Savini, 2018. For example, a survey in Switzerland found that organic farmers use on average between 3% and 80% of the maximum permitted amount of copper depending on the crop, indicating a high awareness among farmers of the need to reduce copper use (Speiser et al., 2015). ...
... Even though various tools and strategies to reduce copper-based plant protection products, such as resistant varieties, cultural measures, decision support systems and alternative plant protection products are available for farmers (Finckh et al., 2015), completely abandoning copper fungicides would lead to high yield losses in many crops at the time being (Kühne et al., 2017). To develop strategies and pathways for a complete phasing out of copper-based plant protection products, policy makers need information on the current dependency on copper-based plant protection products, the implementation of alternative strategies, and the need for copper alternatives in European organic crop production. ...
... Switzerland (Speiser et al., 2015) or Germany (Kühne et al., 2017)) or on specific crops (e.g. olives, ...
Preprint
Full-text available
Reduction of copper-based fungicides with the final aim of phasing out has a high priority in European policy as well as in organic agriculture. Our survey aims at providing an overview of the current use of copper-based plant protection products in European organic agriculture and the need for alternatives to allow policy makers to develop strategies for a complete phasing out. Due to a lack of centralized databases on pesticide use, our survey combines expert knowledge on permitted and real copper use per crop and country with statistics on organic area. In the 12 surveyed countries, covering together 83% of the European organically managed horticultural area, we calculated approximately 3258 t copper metal per year are consumed by organic agriculture, equalling to 53% of the permitted annual dosage. This amount is split between olives (1263 t y ⁻¹ , 39%), grapevine (990t y ⁻¹ , 30%), and almonds (317 t y ⁻¹ , 10%), followed by other crops with much smaller annual uses (<80 t y ⁻¹ ). Potato, usually considered a highly demanding plant for copper inputs, only uses 39 t y ⁻¹ of copper per year. In 56% of the allowed cases (countries × crops), farmers use less than half of the allowed amount, and in 27% less than a quarter, with some variability between countries. Considering the large volumes of copper used annually, replacement of copper seems only feasible if all preventive strategies from the crop protection pyramid are fully implemented and several affordable alternative plant protection products are successfully brought to the market.
... Copper is widely used both in conventional and organic farming systems worldwide (Ostandie et al., 2021). Copper acts as a broadspectrum biocide and is used to control several pathogens, including V. inaequalis, in Integrated Pest Management as well as in organic production systems (Kuehne et al., 2017;Lamichhane et al., 2018). As an essential nutrient element, copper has important functions within plants (e.g., for photosynthesis). ...
... Thus, copper application has become an ecological and political concern in many places, and its application in organic production has already been restricted in some European countries (Holb & Kunz, 2016). Since there is no complete alternative or economic replacement for copper use in organic farming, reducing copper loads in horticultural production systems is seen as a potential strategy to avoid copper accumulation on farmland (Holb & Kunz, 2016;Kuehne et al., 2017;Tamm et al., 2022). ...
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The wetting behaviour of the spray and the biological efficacy of Cu2+ active ingredients in agrochemical formulations may be enhanced by tank‐mix additives. We investigated how three BREAK‐THRU® additives (BT301: biodegradable, BT133 and BT420: bio‐based and biodegradable) tank‐mixed with commercial copper preparations influenced the spray distribution, leaf uptake and biological efficacy of copper additive mixtures against apple scab and apple powdery mildew under controlled conditions. We quantified the synergetic effects of these additives in foliar applications. In addition, we determined the phytotoxic potential and evaluated their impacts on photosynthetic activity, non‐photochemical quenching and ROS activity. The additives BT301 and BT420 strongly reduced surface tension and contact angle of copper treatments. The fluorescence observations revealed that BT301 achieved better spreading of copper formulation with more complete coverage of the leaf surface than BT420 and BT133, whereas “coffee‐ring” spreading was observed with BT133. The additive BT301 showed an increase in relative fluorescence area, indicating higher ROS production as a signal of intra‐cellular tissue activity. The photochemical efficiency of photosystem II (Fv/Fm) was not negatively influenced by copper or additive treatment. Thus, we observed no phytotoxic effects of copper‐additive mixtures on apple leaves at treatment doses of 4 g Cu2+ L‐1. All copper treatments reduced apple scab infections significantly, by 53‐76%. Interestingly, addition of BT301 to copper preparations showed the strongest biological efficacy (83% reduction) against V. inaequalis, whereas addition of BT420 showed the strongest effect against P. leucotricha (89% infection reduction). The synergetic effects of additives on the biological efficacy without phytotoxic effects on plants may have potential for reducing copper loads in horticultural production systems. This article is protected by copyright. All rights reserved.
... In case of organic farming, copper compounds are widely used to fight fungal disease. Kuehne et al. [9] estimate the amount of copper compounds used in German conventional apple farming in the year 2013 to 1.4 kg ha −1 , and, nearly identical, to 1.5 kg ha −1 in organic farming. However, in other crops, e.g. ...
... grapes, the usage of copper compounds increases from 0.8 in conventional agricultural farming to 2.29 kg ha −1 in organic farming. In total, 84.4 t of copper compounds were applied in conventional farming and 26.5 t in organic farming [9]. This massive input of copper-natural Cu concentrations range from 20 up to 100 mg Cu kg −1 soil depending on soil type [10,11] may lead to accumulation in the environment: data from vineyards in France prove that concentrations up to 1500 mg Cu kg −1 soil can be reached [12]. ...
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The constantly increasing demand for agricultural produce from organic and conventional farming calls for new, sustainable, and biocompatible solutions for crop protection. The overuse of fungicides leading to contamination of both produce and environment and the emergence of plant pathogenic fungi that are resistant to conventional treatments warrant the need for new methods to combat fungal infections in the field. We here deliver the follow-up study to our research on the Photodynamic Inactivation (PDI) of plant pathogenic bacteria (Glueck et al. in Photochem Photobiol Sci 18(7):1700–1708, 2019) by expanding the scope to fungal pathogens. Both fungal species employed in this study— Alternaria solani and Botrytis cinerea —cause substantial crop and economic losses. Sodium magnesium chlorophyllin (Chl, approved as food additive E140) in combination with Na 2 EDTA and the chlorin e6 derivative B17-0024 holding cationic moieties serve as eco-friendly photoactive compounds. Effectiveness of the antifungal PDI was measured by inhibition of growth of mycelial spheres (average diameter 2–3 mm) after incubation with the photosensitizer for 100 min and subsequent illumination using a LED array (395 nm, 106.6 J cm ⁻² ). One hundred micromolar Chl combined with 5 mM Na 2 EDTA was able to successfully photokill 94.1% of A. solani and 91.7% of B. cinerea samples. PDI based on B17-0024 can completely inactivate A. solani at 10 times lower concentration (10 µM); however, for B. cinerea , the concentration required for complete eradication was similar to that of Chl with Na 2 EDTA (100 µM). Using a plant compatibility assay based on Fragaria vesca, we further demonstrate that both photosensitizers neither affect host plant development nor cause significant leaf damage. The plants were sprayed with 300 µL of treatment solution used for PDI (one or three treatments on consecutive days) and plant growth was monitored for 21 days. Only minor leaf damage was observed in samples exposed to the chelators Na 2 EDTA and polyaspartic acid, but overall plant development was unaffected. In conclusion, our results suggest that sodium magnesium chlorophyllin in combination with EDTA and B17-0024 could serve as effective and safe photofungicides. Graphical abstract
... fractions, especially in the north and central parts of the country, can be explained by the application of coppercontaining pesticides. Copper pesticides play an important role in plant protection and are used to control fungal and bacterial diseases, such as grapes downy mildew, downy mildew of hops, apple scab, firelight, and potato late blight (Kuehne et al. 2017). The highest content of V was determined in Comrat (18.8 mg/kg) and Balti (18.5 mg/g) while in rural areas its content changed in the range 2.4-9.3 mg/kg. ...
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... There are many copper compounds that are best known for plum rescue, such as copper sulfate, copper oxychloride and copper hydroxide (Kuehne et al. 2017). Only two copper-containing fungicides have been registered for industrial plum plants, which poses the issue of investigating their ultimate effects during changes occurring in the surroundings. ...
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All details about our chapter are available here: https://www.routledge.com/Handbook-of-Plum-Fruit-Production-Postharvest-Science-and-Processing/Gull-Nayik-Wani-Nanda/p/book/9781032062426#
... Looking in more detail at the environmental costs of these inputs, both copper and mineral oils have been used for centuries as highly versatile, cost-effective plant protection products with relatively low toxicity compared to synthetic, chemical pesticides used in conventional agriculture [16,17]. However, copper persists in the environment and may accumulate in the soil, negatively affecting soil biota [18,19]. The mining of copper is also a highly environment degrading activity. ...
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Information about how copper is mobilised in soil can be obtained using sequential extraction method. Four different distribution patterns could be determined analysis soil samples of 78 vine growing areas. These four patterns are different depending on the fraction of the sequential extraction method in which the highest extractable amount of copper is extracted. However, they have in common, that always less than 10% of the total copper content is easily mobilized. The most investigated areas show a high amount of aged and mineralized copper content which is higher than the potential mobile copper content. In areas where more than 60% of the total copper is potentially available is a greater risk that the copper can be mobilized than in areas which have a very high proportion of mineralized or aged copper. The frequency of occurence of the different distribution patterns of the analyzed areas vary depending on the sample area and the pedological parameter. Significant influencing factors are the copper content, soil texture (sand content) and the pH-value. The potential mobile copper content as well as specific soil conditions, which raise the metal mobility are important to develop criterions for the selection of endangered areas for the implementation of RL 2009/37/EG. These criteria will be proposed to the Management Authority as a decision support for the establishment of programs for “vulnerable zones”, where the contamination of soil with copper causes for concern. © 2015 Centro de Estudos da Faculdade de Enfermagem da UERJ. All rights reserved.
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The samplings carried out in the years 2009 and 2010 were designed to provide a survey of the copper contents of soils of vine culturing regions in Germany. The data base received may be used for additional more specific surveys and the identification of sites appropriate for long term monitoring as well. It is also considered as a prerequisite for the identification of sites suitable for the assessment of effects of copper soil contamination to soil dwelling organisms in terms of the “strategy paper concerning further copper application in agriculture, especially in organic farming.” 2087 single samples from the soil horizon to 5 cm and to 20 cm were taken from 85 ecologically and conventionally managed vine yards. The sampling aims to get a representative survey of load distribution as a prerequisite of a monitoring program to be performed on selected sampling locations combining exposure analysis and identification of sensitive indicator species of the particular earthworm coenoses. On the basis of total contents, copper load and distribution on test and reference areas of German cultivation sites is shown. The influence of plant cover between the rows on the copper distribution pattern in the soil horizons to 5 cm and to 20 cm and the differences of samples taken along the cultivation rows and between them is discussed. Samples were taken from 56 ecologically and 29 conventionally managed sites, onsisting of an area under cultivation (test area), an area having been under cultivation in the past (reference), an area never having been under cultivation indicating natural occurrance (control). Total copper contents of test and reference areas (581 soil samples) from the soil horizon 0–20 cm were analyzed and presented as minimum, maximum, mean and percentiles. The load distribution survey in combination with management history and literature data verifies that load peaks result from high copper input in the years 1890 to 1940, when up to 50 kg copper per ha and year was applied to control fungal diseases in viticulture. By means of the data, generated in the survey concerning load situation, site description and duration of management, 15 cultivation sites representing by their properties a typical site, and fulfilling the site specific requirements for a biological sampling on species abundance of lumbricidae are proposed as an instrument of risk assessment for soil dwelling organisms. The transfer of knowledge into practice is ensured by close co-operation with organic farming associations and expert discussions with involved institutions. The derived contamination scenario will be provided to agencies taking part in the authorization process.
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Soil samples were taken from 9 conventionally and 4 organically managed hop growing sites, considering all aspects that are relevant for a representative assessment of copper loads. The result of this survey is intended to enable the selection of characteristical cultivation types for each site, which, in combination with a refined exposure analysis, are a prerequisite for the assessment of the effects of copper on earthworm coenoses. Based on total contents, the copper load and its distribution on test and reference fields of German hop cultivation sites is presented. Additionally, the heavy metal content was determined in general, and differences in copper contents between and within hop rows were identified. The management history of the hop sites led to additional heavy metal soil contamination (As, Cr, Pb, Zn, V). Due to different cultural measures exercised in the past, the analyzed total heavy metal contents differ between growing regions. Comparing literature with managing history and current management, it is obvious that peaks of contamination result from applications between 1924 and 1965, when for the control of plant diseases up to 60 kg copper per ha and year were used. The collected data concerning load situation, site description and duration of management suggest that three hop sites are appropriate for a biological assessment of soil quality and its recent impact on earthworm coenoses.
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In organic potato (Solanum tuberosum) production in Europe, solely copper-based fungicides allow to directly control late blight (caused by Phytophthora infestans). Due to environmental concerns, the use of copper (Cu) fungicides has to be as efficiently as possible to reduce annual consumption. This can be achieved either by reducing the dose per application or by decreasing the numbers of sprays. Between 2005 to 2009, six field trials were conducted at two sites (3 each) in northern Germany in order to (a) determine the efficacy of a copper fungicide (copper hydroxide) at reduced rates compared to the common practise of the most important German organic farmers' associations (3 kg Cu ha-1), and (b) to evaluate the copper reduction potential of an application strategy based on a decision support system (DSS). A clear dose-response relationship with reduced rates of copper hydroxide was not consistent over trials and strategies although there was clear evidence for a considerable potential to reduce Cu rates compared to the amount of 3 kg Cu ha-1. However, different degrees of late blight pressure strongly affected the efficacy of the Cu fungicide in individual years. Under less late blight pressure, a reduction to 1.25 kg Cu ha-1 applied throughout the season was possible without significant loss in efficacy compared to the typical spraying of 2.5 or 3.0 kg Cu ha-1. Due to a higher risk of decreasing efficacy, reducing Cu hydroxide supply was only possible to an amount of 2.0-2.5 kg Cu ha-1 under moderate disease pressure while high late blight pressure in 2007 did not allow a Cu reduction to this extent. Even the highest amount of 3.0 kg Cu ha-1 only decreased the disease by 18% in one single case. Consequently, yields were not consistent, but depended on year, site and late blight pressure. On average over rates and strategies, Cu application increased yields by 15%. In addition, the results revealed the clear tendency that reducing Cu amounts did not impair tuber yield. A spray schedule based on the new German DSS ÖKOSIMPHYT increased effectiveness of Cu sprays, reduced numbers of sprays and the total amount of Cu per year, even under moderate and high late blight pressure. Therefore, we conclude that the DSS has the potential for further optimization. Knowledge of actual late blight pressure, as provided by ÖKOSIMPHYT, is necessary to optimize the use of Cu fungicides allowing both to ensure the site-specific tuber yield potential and to reduce the CU application amounts.
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Ziel des dreijährigen Projekts war es, Schlüsselparameter der bisher unter europäischen Bedingungen nur wenig erforschten Regenfleckenkrankheit (RFK) zu erarbeiten. In den Regionen Altes Land und Bodensee dominierte in allen drei Versuchsjahren (2007 – 2009) ein und derselbe RFK-Erreger, Peltaster sp.. Weitere RFK-Erreger sowie der Erreger der Fliegenschmutzkrankheit (FSK), Schizothyrium pomi, kamen nur sporadisch vor und sind wahrscheinlich für die Bekämpfung der Symptome derzeit ohne Bedeutung. In beiden Regionen ist die RFK fast ausschließlich auf ökologisch bewirtschaftete Anlagen beschränkt. Eine Besiedlung von Obstanlagen durch RFK-Erreger findet zunächst von außen statt, kann dann aber in den darauf folgenden Jahren durch endogenes Inokulum getragen werden. Fruchtmumien spielen eine Rolle als endogene Infektionsquellen. Umfangreiche Versuche zur Präzisierung der Infektionsbedingungen haben ergeben, dass eine Besiedlung der jungen Früchte bereits zum sehr frühen Zeitpunkt (T-Stadium, BBCH 74) und danach während des gesamten weiteren Saisonverlaufs erfolgen kann. Die Stärke der Symptomausprägung zur Ernte ist in erster Linie davon abhängig, wie lange die Früchte den natürlichen Infektionsbedingungen ausgesetzt waren. Je später in der Saison Infektionen stattfinden, desto weniger Zeit haben die RFK-Pilze für die Besiedlung und Ausbreitung auf der Frucht, so dass späte Infektionen i.d.R. nicht mehr zu starken Befallsgraden führen. Zur Ausprägung von RFK-Symptomen ist Blattfeuchte, auch in Form von Taubildung, ausreichend, jedoch wird die Symptomausbildung mit zunehmenden Niederschlagsmengen deutlich beschleunigt. Sind erste RFK-Symptome in einer Anlage sichtbar, verkürzt sich die zur Inkubation notwendige kumulative Blattnässedauer von etwa 250 auf unter 150 Stunden. Die RFK-Erreger scheinen eine mehrwöchige Trockenphase unbeschadet überdauern zu können. Apfelsorten zeigen deutliche Unterschiede in der Ausprägung der RFK-Symptome. Die Ursachen hierfür müssen in weiteren Untersuchungen geklärt werden.